Nordic Society Oikos

Latitudinal Gradients in Species Diversity: The Search for the Primary CauseAuthor(s): Klaus RohdeSource: Oikos, Vol. 65, No. 3 (Dec., 1992), pp. 514-527Published by: Blackwell Publishing on behalf of Nordic Society OikosStable URL: http://www.jstor.org/stable/3545569Accessed: 31/01/2010 15:24

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OIKOS 65: 514-527. Copenhagen 1992

MINI- REVIEW

Minireviews provides an opportunity to summarize existing knowledge of selected ecological areas, with special emphasis on current topics where rapid and significant advances are occurring. Reviews should be concise and not too wide-ranging. All key references should be cited. A summary is required.

Latitudinal gradients in species diversity: the search for the primary cause

Klaus Rohde

Rohde, K. 1992. Latitudinal gradients in species diversity: the search for the primary cause. - Oikos 65: 514-527.

Hypotheses that attempt to explain latitudinal gradients in species diversity are reviewed. Some hypotheses are circular, i.e. they are based on the assumption that some taxa have greater diversity in the tropics. These include explanations assuming different degrees of competition, mutualism, predation, epiphyte load, epidemics, biotic spatial heterogeneity, host diversity, population size, niche width, population growth rate, environmental harshness, and patchiness at different latitudes. Other explanations are not supported by sufficient evidence, i.e. there is no consistent correlation between species diversity and environmental stability, environmental predictability, productivity, abiotic rarefaction, physical heterogeneity, latitudinal decrease in the angle of the sun above the horizon, area, aridity, seasonality, number of habitats, and latitudinal ranges. The ecological and evolutionary time hypotheses, as usually understood, also cannot explain the gradients, nor does the temperature dependence of chemical reactions permit predictions on species richness. Only differ- ences in solar energy are consistently correlated with diversity gradients along lat- itude, altitude and perhaps depth. It is concluded that greater species diversity is due to greater "effective" evolutionary time (evolutionary speed) in the tropics, probably as the result of shorter generation times, faster mutation rates, and faster selection at greater temperatures. There is an urgent need for experimental studies of temper- ature effects on speed of selection.

K. Rohde, Dept of Zoology, Univ. of New England, Armidale, NSW 2351, Australia.

Even approximate estimates of species numbers on earth cannot be given (May 1990), but it is well estab- lished that the tropics harbour many more species than colder environments. Such latitudinal gradients in spe- cies richness are among the most universal features of nature and have been discussed by many authors (e.g. Dobzhansky 1950, Kuznezov 1957, Fischer 1960, Klopfer and MacArthur 1961, MacArthur 1965, 1969, 1972, Pianka 1966, 1988, 1989, Ricklefs 1973, Pielou 1975, Connell 1978, Rohde 1978a, b, 1980b, 1984, 1989, Schall and Pianka 1978, Huston 1979, Parsons and Bock

Accepted 6 May 1992 ? OIKOS

1979, Alekseev 1982, Thiery 1982, Brown and Gibson 1983, Krebs 1985, Begon et al. 1986, Stevens 1989, Hengeveld 1990) (examples in Figs 1 and 2). They have been shown to occur in habitats as diverse as the open ocean, coasts, rainforests, deserts, rivers, lakes, etc. Among the few exceptions are ichneumonid parasitoids (Owen and Owen 1974, Rathke and Price 1976, Janzen 1981; but possibly not all parasitoids, see Hespenheide 1979), helminths of marine mammals (Delyamure, cit. Rohde 1982; Table 1), and cold adapted smaller taxa. In spite of their importance, authors cannot agree on an

514 OIKOS 65:3 (1992)

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explanation of the gradients. According to Pianka

(1989), the problem of great tropical species diversity "is seriously complicated by multiple causality as well as

very probably being ahead of its time". In this paper, I give a brief review of the hypotheses

that attempt to explain latitudinal diversity gradients, with special reference to recent work. Emphasis is not on the various factors that bring about local differences in diversity and that may enhance latitudinal gradients secondarily, but on the primary cause(s) of the lat- itudinal gradients, if such causes do indeed exist. For this reason, papers and books dealing exclusively with local diversity, such as Tilman (1982, 1988), Janzen (1987), Hubbell et al. (1990), and Wilson (1990) and with ecological factors that may affect diversity but are not directly relevant to latitudinal gradients, such as Hubbell and Johnson (1977), Wright and Hubbell

(1983), Hubbell and Foster (1986), and Howe (1990) are not discussed. No attempt is made to distinguish a, 3 and y diversity (e.g. Brown and Gibson 1983), and species numbers, diversity and richness are used inter-

changeably. This review restricts itself to giving only essential arguments against each hypothesis, i.e. such

arguments that clearly show that a hypothesis cannot

give a general explanation of latitudinal diversity gra- dients.

PACIFIC

ATLANTIC

5 10 15 20 25 Mean Annual Sea Surface Temperature (?C)

Fig. 2. Relative species diversity (number of parasite species per host species) of monogenean gill parasites of teleost fish in the Pacific and Atlantic Oceans. Broken lines and open circles: total number of Monogenea species/total number of host spe- cies. Continuous lines and filled circles: species occurring in x host species counted x times. Bar: + S.E. Modified from Rohde 1986.

A common gradient is likely to have a common explanation As stated by several authors, an almost universal pat- tern must have some common explanation (e.g. Pianka 1966, Rohde 1978a). Ricklefs (1973) has summarized this view as follows:

"The general latitudinal pattern in species numbers must be related to some climatic factor, or combination of factors, that changes in a consistent manner with latitude. Several factors could serve as suitable candi- dates: average temperature, annual rainfall, and sea- sonality, to name a few, but ecologists have failed to find a convincing link between organic diversity and patterns in the physical environment."

Table 1. Helminth species of pinnipeds and cetaceans at different latitudes. From Rohde (1982) according to Dogiel.

Biogeographical zone Trematodes Cestodes Nematodes Acantho- Total cephalans

Arctic 6 7 9 3 25 Boreal 30 24 31 9 94 Tropical 7 2 18 4 31 Antiboreal 0 9 21 8 38 Antartic 1 7 5 1 14

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515 OIKOS 65:3 (1992)

Table 2. Circular 'explanations' of latitudinal gradients in spe- cies diversity. Only some key references are given (authors who proposed or discussed the hypotheses).

Competition (Dobzhansky 1950, Pianka 1966, Huston 1979). Mutualism (Brown and Gibson 1983). Predation (Paine 1966, Pianka 1966, Janzen 1970, Rathke and

Price 1976, Hubbell 1980). Epidemics. Biotic spatial heterogeneity (Huston 1979, Thiollay 1990). Population size (Boucot 1975, Rohde 1978a). Niche width (Ben-Eliahu and Safriel 1982, Brown and Gibson

1983). Population growth rate (Huston 1979). Patchiness (McCoy and Connor 1980). Epiphyte load (Strong 1977). Host diversity (Rohde 1989). Harshness (Thiery 1982, Brown and Gibson 1983, Begon et al.

1986).

Likewise, Brown and Gibson (1983) concluded that "ul-

timately, all general patterns of diversity must be attri- buted to physical causes, either historical perturbations or contemporary variation in the physical environment" and "hypotheses that invoke biotic interactions must

always be at least secondary explanations of diversity patterns", and according to Pianka (1988) "Ultimately a

thorough understanding of patterns in diversity requires knowledge of primary-level mechanisms".

In looking for a common cause, care has to be taken not to confuse correlation with causation (Pianka 1966), although strong correlation between diversity and some

parameter may be strongly indicative of a possible cause.

Some explanations are circular Table 2 lists "explanations" for the gradients given by some authors that are obviously circular, dependent on a greater diversity of at least some groups of organisms at low latitudes. For example, there is evidence that, under certain conditions, increased competition, mu- tualism, predation and biotic spatial heterogeneity are associated with increased species diversity. However, with regard to increased species richness in the tropics, the main problem is not to demonstrate such an associ- ation but to answer the question of the origin of the greater numbers of competitors, predators, or orga- nisms (such as corals and algae on coral reefs) respon- sible for creating complex habitats for other species. As put by Begon et al. (1986) with regard to predation, "it cannot be the root cause, since predation is itself an attribute of the community". The same argument ap- plies to parasites or microorganisms responsible for epi- demics, and similarly, reduced population size and

niche width cannot be the cause but must be the result of denser species packing. Furthermore, populations are not always smaller and niches not always narrower in the tropics, indicated for instance by the finding that at least in some groups, host ranges of parasites are not narrower in the tropics (Fig. 3) (see also Rohde 1978c, Beaver 1979) and microhabitat width is not greater in

species poor communities (Rohde 1981) (for a fuller discussion of latitudinal gradients in niche width see Rohde 1989). The dynamic equilibrium model of Hus- ton (1979) predicts that "a major determinant of di-

versity in nonequilibrium (referring to competitive equi- librium) situations is the level of population growth rates of competitors. At low to intermediate frequencies of population reduction, low growth rates allow the maintenance of diversity by slowing the approach to competitive equilibrium and enhancing the effect of factors that tend to prevent competitive exclusion". Huston concluded that his model could explain at least part of the latitudinal gradient in species diversity, be- cause in the tropics soil nutrients are reduced and rates of respiration increased, resulting in lower population growth rates in the tropics. Huston's prediction seems to be supported by the fact that, in tropical forests, much of the nutrients is indeed found in the plants, whereas a greater proportion of the nutrients is found in the soil of high latitude forests. However, as with the hypotheses discussed above, this difference is not due to some underlying physical factor but at least partly the result of the greater diversity of plants. Also, the model does not hold for aquatic environments.

McCoy and Connor (1980) stressed the importance of "patchiness" in increasing regional species diversity at low latitudes. High patchiness may indeed occur in trop- ical rainforests, etc., but there is no universal gradient in patchiness (it is absent for example in the open ocean, although species numbers of open ocean fishes and of plankton decrease with latitude), and - where it is found - it is due to the diversity gradient and not its cause (see for instance the increased patchiness result- ing from higher tree fall rates in tropical forests dis- cussed in the following paragraph).

100 o '

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Fig. 3. Host ranges of marine Monogenea (o) and trematodes (x) at different latitudes as characterized by means of annual sea surface temperatures. Note that even in cold seas, where host ranges of trematodes are wide, only few host species are heavily infected (Rohde 1980c). Modified from Rohde 1978c.

OIKOS 65:3 (1992)

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Table 3. "Explanations" of latitudinal gradients in species di- versity insufficiently supported by evidence. Only some key references are given (authors who proposed or discussed the hypotheses).

Environmental stability (Klopfer 1959, Klopfer and MacAr- thur 1961, Connell and Orias 1964, MacArthur 1965, Pianka 1966, Margalef 1969, Sanders 1969, Thiery 1982, Staff and Powell 1988).

Environmental predictability (contingency) (Slobodkin and Sanders 1969, Janzen 1970, Sale 1977, Huston 1979, Thiery 1982, Begon et al. 1986).

Productivity (Pianka 1966, MacArthur 1969, Brown and Gib- son 1983, Begon et al. 1986, Currie 1991).

Abiotic rarefaction (Dobzansky 1950, Connell 1978). Physical heterogeneity (Pianka 1966, Huston 1979, Brown and

Gibson 1983, Begon et al. 1986). Latitudinal decrease in the angle of the sun above the horizon

(Terborgh 1985). Area (Connor and McCoy 1979, Currie 1991). Aridity (Begon et al. 1986). Seasonality (Begon et al. 1986). Number of habitats (Pianka 1966). Latitudinal ranges (Rapoport's rule) (Rapoport 1982, Pianka

1989, Stevens 1989, Rohde et al. in press).

Strong (1977) pointed out that vine and epiphyte loads of wet, lowland forest canopy increase dramat-

ically in the tropics, and this may be an important cause of high tree fall rates in tropical forests, producing a

perennial patchwork of disturbance and maintaining the forests as a perpetual preclimax mosaic. Diversity is increased by reducing the frequency of long-term com-

petitive interactions between adjacent individuals. The effect would be similar to that caused by predation but - as with the predation hypothesis - it depends at least partly on a greater diversity of epiphytes in the tropics. Furthermore, it cannot explain the latitudinal gradient for aquatic and non-forest terrestrial environments.

Rohde (1989) demonstrated that diversity of the host

group is largely responsible for species richness of cope- pods parasitizing scombrid fishes, a phenomenon that has been shown for several groups of parasites and is known as Eichler's rule (see Rohde 1982). Since host diversity is generally greater at low latitudes, it may at least partly explain greater tropical parasite diversity. However, this gives no explanation for the host plant or animal diversity gradients.

Some authors have tried to explain lower diversity in certain habitats as due to greater "harshness" leading to low colonization and speciation rates and/or high extinc- tion rates (see discussions in Thiery 1982 and Brown and Gibson 1983, references therein). However, the concept of "harshness" cannot be defined without circu- lar reasoning. "Thinking of the tropics as benign and the polar region as harsh is only a habit of thought; it results from the fact that life is more abundant in the tropics..." (Pielou 1979) (see also Begon et al. 1986). Several of the factors listed in Table 3 could contribute to "harsh- ness".

Some explanations are not supported by sufficient evidence Table 3 lists "explanations" not sufficiently supported by evidence. Thus, although environmental stability and predictability are known to be great in some parts of the tropics, there may be extreme variations in tem- perature, salinity and currents in tropical shallow wa- ters, for instance on high diversity coral reefs. Such

variability may be quite unpredictable, such as in the case of tropical storms. Staff and Powell (1988) found no relationship between increased species richness and reduced environmental variability in living benthic com- munities. Productivity also is not consistently correlated with species diversity. It is low, for example, in some tropical seas with high diversity. Some authors have shown peaks of diversity at intermediate levels of pro- ductivity (examples in Begon et al. 1986.) There is

progressive decline in diversity with eutrophication of lakes, etc. and some of the most diverse plant communi- ties are found on nutrient-poor soils, where nearby communities on richer soil have lower diversity (ibid.). There is no evidence that abiotic rarefaction (reduction in population density by physical events like storms, dry or cold periods, etc.) differs between high and low latitudes, and the intermediate disturbance hypothesis, according to which repeated external disturbances cre- ate opportunities for a variety of species (e.g. Connell 1978) cannot therefore account for the latitudinal gra- dients. There also is no general latitudinal gradient in

physical complexity (heterogeneity). The great number of islands in the warm western Pacific represents a case of great physical heterogeneity in tropical waters, but such large numbers of islands are absent in the tropical Atlantic, and there is a distinct diversity gradient of plankton in the open ocean, without corresponding gra- dients in heterogeneity. For North American verte- brates, Currie (1991) found only a weak correlation between species richness and spatial "variability".

A special case of structural complexity at different latitudes leading to differences in species richness has been discussed by Terborgh (1985), due to changes in the angle of incidence of light with latitude. As a conse- quence of different light regimes, tree crowns of high latitudes are narrowly conical in profile, whereas those in the tropics tend to be planar or shallowly dome- shaped. In high latitude forests, therefore, light is ad- mitted at sharply inclined angles which do not permit growth of a second tree layer. In the tropics, on the other hand, light penetrates the canopy at shallower angles, permitting growth of a second layer. It is clear that this is a very special case not applicable to most environments, particularly aquatic ones.

An effect of area has repeatedly been shown to be responsible for local differences in species diversity, particularly in island biogeography. Wright (1983) found that energy x area was the best predictor of

OIKOS 65:3 (1992) 517

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Fig 4. Number of species of gill Monogenea found on marine teleost fish species of different maximum total length. x = southeastern Australia; ? = Pacific Coast of Canada. Only those fish species included of which at least 20 specimens examined. Modified from Rohde 1989.

species diversity on islands varying widely in size and latitude. In contrast, Currie (1991) found that for the vertebrates of continental North America, only a very weak area effect existed (but area varied by less than a factor of two for most of his quadrats). Rohde (1989) examined the effect of area on parasites of marine tele- osts, as indicated by size of host species (Fig. 4), ge- ographical range of host species and geographical area occupied by whole host faunas and concluded that area is not predominant in determining species richness in marine parasites. Neither the surface nor the shelf areas of the northern Pacific are greater than those of the northern Atlantic but nevertheless have a three times larger relative species diversity (parasites per host spe- cies) of Monogenea (Rohde 1986) (Fig. 2). Tropical America has a smaller area than North America and tropical Asia is much smaller than the more northern parts of that continent. Hence, not all tropical regions have a larger area than cold-temperate zones and area cannot give a general explanation of the latitudinal di- versity gradients.

Concerning aridity, there is indeed often a clear de- crease of productivity with aridity (e.g. Begon et al. 1986), although more productive habitats do not neces- sarily have more species (see above). Currie's (1991) analysis of North American vertebrates shows that greatest species richness of homeotherms occurs in high-energy, dry, mountainous areas. Most impor- tantly, on a global scale, diversity gradients are also found in aquatic environments.

Pielou (1979) gave an example of a presumed sea- sonal effect on species diversity, in predatory gastro- pods in the northern Atlantic (from the study by Taylor and Taylor). In the North Atlantic, at about 40?N, there is a switch from continuous to seasonal primary produc- tivity, and at that boundary an abrupt change in the number of taxa occurs particularly in the eastern North Atlantic. The larger number south of the boundary is explained by an unvarying supply of many prey species which permit coexistence of many predatory species

with highly specialized diets. In contrast, Currie (1991), in his detailed study of North American vertebrates, concluded that "one can reject the hypothesis that an- nual variability of climate per se has an important effect on richness", i.e. there is no consistent correlation be- tween seasonality and species diversity.

Some parts of the tropics have a greater number of habitats (e.g. from warm to temperate to cold along an altitudinal gradient) than colder environments, as pointed out by Simpson (see Pianka 1966), but this does not apply to many shallow seas, flatlands and other habitats. Therefore, it cannot be a general explanation of latitudinal gradients in species diversity.

Stevens (1989) compared latitudinal ranges of North American trees, marine molluscs with hard body parts, freshwater and coastal fishes, reptiles and amphibians, and mammals between 25 and 80?N and found that high latitude species had wider latitudinal ranges than low latitude species (Fig. 5), a phenomenon he called Rapo- port's rule after Rapoport, who had referred to the correlation while describing the degree of geographical overlap between subspecies (Rapoport 1982). He con- cluded that existence of the rule suggests narrower envi- ronmental tolerances of tropical than of temperate/po- lar organisms and went on to speculate that equal dis- persal abilities of the two groups would place more tropical organisms out of their preferred habitats than higher-latitude species, and that a constant input of "accidentals" from adjacent habitats would artificially inflate species numbers and inhibit competitive exclu- sion. This would be a case of "mass effect", i.e. the establishment of species in sites where they cannot be

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Fig 5. Mean latitudinal range of North American marine mol- luscs with hard body parts. Note that for each latitudinal 5? band, all species occurring within that band irrespective of the midpoint of their distribution, were considered, i.e. a species with a range of 50? appears in 10 or 11 bands. Modified from Stevens 1989.

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self-maintaining, shown to occur in plant communities on a local scale by Shmida and Wilson (1985).

Rohde et al. (in press) have shown that Rapoport's rule indeed applies to North American freshwater and coastal fish above a latitude of 40?N, but it does not apply to marine teleosts in tropical waters (Figs 6, 7) (which have a very distinct latitudinal gradient in spe- cies diversity, Fig. 1). The rule could be simulated when it was assumed that species numbers decrease with in- creasing latitude, and that species at all latitudes have narrow ranges except for a few low latitude ones which reach into high latitudes, i.e. the rule may be an artefact at least for some taxa. Furthermore, input of "acciden- tals" from adjacent habitats, although increasing local diversity, would not inflate total diversity in the tropics, and "Thorson's rule" (according to which tropical ben- thic invertebrates tend to have pelagic dispersal larvae, whereas cold-water species have non-pelagic develop- ment) indicates that dispersal abilities are not equal but greater in tropical species (at least of benthic inver- tebrates) (Rohde 1989). Also, many large groups of animals, such as families of fish and hermatypic corals, are restricted to the tropics, and there is no evidence that there is a major "spill-over" of species from high to low latitudes. On the contrary, fossil evidence suggests that "adaptations which permit the occupation of major new niches and thus lead eventually to the development of higher taxa, take place in the tropics" (Stehli et al. 1969).

v

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Ecological and evolutionary time hypotheses cannot give a general explanation The time hypotheses assume that communities diversify in time. "Structure, in general, becomes more rich, as time passes..." (Margalef 1963). Pianka (1966, 1988) distinguishes an ecological and evolutionary time hy- pothesis (Table 4). The former claims that species for certain habitats exist but have not yet had time to spread into them, whereas the latter applies to longer time spans and claims that species for certain habitats have not yet had time to evolve. Pianka (1988) gives patches of forest burned by lightening or isolated lakes into which available species have not yet spread, as

Table 4. Explanations of latitudinal gradients in species di- versity based on time or direct solar effects. Only some key references are given (authors who proposed or discussed the hypotheses).

Ecological time (Fischer 1960, Pianka 1966, 1988, Rohde 1978a, Brown and Gibson 1983).

Evolutionary time (Pianka 1966, 1988, Whittaker 1969, Rohde 1978a, Pielou 1979, Thiery 1982, Brown and Gibson 1983).

Temperature dependence of chemical reactions (Alekseev 1982).

Solar energy (Currie 1991). Greater 'effective' evolutionary time (evolutionary speed) in

tropics (Rensch 1959, Stehli et al. 1969, Rohde 1978a, b, Thiery 1982).

OIKOS 65:3 (1992)

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examples which can be explained by the ecological time

hypothesis, and the impoverished faunas and floras of areas of recent glaciations and other geological disturb- ances as examples to be explained by the evolutionary time hypothesis. The poorer fauna of the Northern At- lantic compared with the Northern Pacific is supposed to be due to greater effects of glaciation in the former, where barriers like the Asian-North American land-

bridge blocking the advance of the ice were absent (e.g. Rohde 1986). Another example often given is the

poorer tree flora of Northern Europe compared with that of Northern America. Latitudinal shift of trees due to the advancing ice in Europe was blocked by moun- tain ranges extending in an east-western direction. Trees in North America, in contrast, could shift latitudinally because mountain ranges extend predominantly in a north-southern direction, and they could recolonize ar- eas vacated by the ice after the ice age. (However, Currie and Paquin 1987 have argued that tree diversity in Britain is exactly as predicted from the relationship between evapotranspiration and species richness in North America). A richer fauna in old than in more

recently developed lakes (Brooks 1950) provides fur- ther evidence that a time hypothesis can explain some differences in local diversity, but it is doubtful that it can give a general explanation of the diversity gradients, because they are also found where glaciations or similar events had no effect. Furthermore, it is hard to imagine that most marine organisms did not shift latitudinally during a glaciation. This applies especially to marine plankton, but also to pelagic fishes, for which distinct latitudinal gradients in species diversity have been dem- onstrated. It is well known that marine fish may change their distribution much faster than for example trees (a few years vs millenia for the same change, Steele 1991). Connell and Orias (1964) have even argued that tem- perature changes would have greater effects on tropical

or polar regions than at intermediate latitudes, and this is indeed clearly shown by data on paleotemperatures. In the late quaternary, 18 000 years ago, temperature changes in the Atlantic Ocean were greatest between 42?N to 60?N (exceeding 10?C), followed by the tropics (several ?C lower except for a small area in the western Atlantic where temperatures were about 2?C lower than today's); a large temperate region with temperatures similar to today's had simply shifted to the south (McIn- tyre et al. 1976; see also Prell et al. 1976 and Prell and

Hays 1976 for the Caribbean, where temperatures 18000 years ago were reduced by 4-5?C in winter, and by 1-2?C in summer). Eight million years ago in the late miocene, temperatures in surface waters of the equa- torial Pacific Ocean were lower than today's, and in other regions similar to today's temperatures (Savin et al. 1985). Also, mass extinctions in earlier geological eras have occurred in tropical as well as cold envi- ronments, and latitudinal gradients in species diversity have been in existence for at least 270 million years (Stehli et al. 1969). In his study of North American trees and vertebrates, Currie (1991) found that effects of glacial history were barely discernible. His data suggest that tree and vertebrate richness can reach limits (thought to be set by energy) in less than 14 000 years (since the end of the last ice age; at least in North America, probably due to immigration of species that had shifted latitudinally with the glaciation).

One of the assumptions of the evolutionary time hy- pothesis is an increase of species numbers with geolog- ical time. Fossil evidence for such an increase is not as clearcut as might be expected, and different authors have arrived at different conclusions, due to the difficul- ties in obtaining reliable data. Raup (cit. Pielou 1979) has emphasized that one can easily be misled by system- atic biases in the fossil record, and Rohde (1989) has pointed out that fossilized species represent only a small fraction of all animal species and that hardly any para- sites, which represent over half of all animal species, and the many small insects in tropical rainforest cano- pies, can be expected to fossilize (for a fuller account see Rohde 1989). Nevertheless, even the most critical accounts show at least a gradual increase in species numbers (Fig. 8, see discussion in Brown and Gibson 1983, see also Simpson 1969).

Short and long term climatic fluctuations between cold and warm states have occurred for the last 700 million years (Fischer 1981), i.e. evolutionary time has not been greater in the tropics. Hence, the evolutionary time hypothesis can give a satisfactory explanation of the latitudinal gradient in species diversity only if some mechanism explaining differential accumulation of spe- cies at different latitudes is assumed, an aspect dis- cussed below.

OIKOS 65:3 (1992) 520

Time hypotheses can explain differences Temperature-dependence of chemical in species richness between some large reactions does not permit predictions ecosystems at equal latitudes about diversity gradients Although time hypotheses cannot give a general expla- nation of latitudinal gradients in diversity, they can explain the very great differences in species diversity between some ecosystems at the same or similar lat- itudes, such as those between the Atlantic and Indo- Pacific Oceans. Examples of such differences are given in Figs 1 and 2. Not only are species numbers of teleost fishes much greater in the Indo-Pacific than in the At- lantic (Fig. 1), monogenean gill parasites of these fishes also show a marked difference (Fig. 2). Although num- bers of benthic Foraminifera is greater on the Caribbean than on the Pacific side of America (Buzas and Culver 1991), the Indo-Pacific as a whole has been shown by many authors to harbour a much richer flora and fauna of most groups than the Atlantic. The Indo-Pacific dif- fers from the Atlantic in several abiotic parameters: greater size, greater complexity (greater number of is- lands, a larger and more complex coastline, more rivers joining it), and greater age; an explanation of the differ- ences in diversity is therefore difficult to give. Never- theless, Rohde (1986), using an animal group almost entirely restricted to cold-temperate waters and com- paring the North Pacific and North Atlantic, has shown that the greater age of the fauna in the former is the most likely explanation for differences in species di- versity:

The majority of Monogenea of teleost fishes in north- ern cold-temperate waters is comprised of viviparous Gyrodactylidae, which are very rare in warm waters and are therefore unlikely to have spread from low into high latitudes. Relative species diversity (average number of parasite species per host species) of Monogenea in the northern Pacific is more than twice as great as in the northern Atlantic. A species-area relationship or differ- ences in structural complexity cannot explain the differ- ences in diversity, since the northern Pacific is not larger in area than the northern Atlantic and since structural complexity, as indicated by the length of the coastline and the number of islands, also is not greater in the northern Pacific; length of the major rivers draining into the northern Pacific and their discharge rate and annual discharge volume are smaller than those of the northern Atlantic. Rohde (1986) concluded that the differences in diversity are likely to be due to the greater age of the Indo-Pacific (much of geological time vs approximately 150 million years for the Atlantic) and/or the smaller extent of glaciation in the former (continental shelf areas in the northeastern Pacific hardly affected, practi- cally all of the shelf in northern Atlantic covered by ice).

Alekseev (1982) derived the following equation of spe- cies richness

P = Poevt

where

P = total number of species in the system, Po = M/S,

M = Mi(i) + Mo = constant, i,j

Mo = amount of limiting nutrient in the environment, Mi(j) = biomass of the jth species of the ith trophic level, S = average value of constants that characterize the average ratio of mortality to metabolic intensity at 0?C, t = temperature (?C), v = ut / (RTo2), R = gas constant, To = 273K, p[ ranalogous to the activation energy in chemical kinetics. Using empirical data of numbers of marine species in six regions (cold, temperate and trop- ical), he parameterized the equation as P = 400eo'54t. Derivation of the equation shows that the temperature dependence of chemical reactions does not permit pre- dictions about species numbers in environments with different temperatures. Rather, the values in the equa- tion are purely empirical.

Energy is a good predictor of species richness Hutchinson (1959) suggested that energy may deter- mine species diversity (see also Connell and Orias 1964). Consistent with this assumption seems to be Wright's (1983) finding that the product energy x area was the best predictor of species diversity on islands where both island size and latitude varied widely, and Currie's (1991) and Turner's et al. (1987) results from their analyses of North American trees and vertebrates and of British butterflies and moths, respectively.

Turner et al. found temperature and sunshine during the summer months to be most closely correlated with species diversity. Currie divided the North American continent into 336 quadrats (of unequal areas) and esti- mated the number of species of trees, birds, mammals, amphibians and reptiles in each quadrat from various sources. For each quadrat, 21 descriptors of the envi- ronment were estimated and a statistical relationship between the variables sought. Since intensities of com- petition, predation and disturbance are difficult to as- sess, they were not included in the analysis. Correlation of species richness with latitude was strong but not

34 OIKOS 65:3 (1992) 521

Table 5. Numbers of species of Monogenea on the gills of deep and shallow water teleosts in southeastern Australia. Modified from Rohde (1991) with one additional record of a monogenean species from shallow water.

No. of fish species infected No of species Relative species diversity of Monogenea (no. Monogenea species/no.

host species examined)

Deep water (1563 fish of 66 or 67 23 or 24 (35 or 36%) 19 0.28 or 0.29 species 35 families) Shallow water (1892 fish of 46 40 (87%) 84 1.83 species, 26 families)

monotonic (except for reptiles) indicating that not lat- itude per se, but some factor covarying imperfectly with latitude, is the determining factor. Strongest correlation for trees was with actual evapotranspiration (the amount of water that actually evaporates from a sur- face) (see also Currie and Paquin (1987)). The three strongest correlates of species richness of each of the vertebrates classes were annual potential evapotranspi- ration (PET), solar radiation and mean annual temper- ature, the last two explaining nearly as much variance as PET. PET is interpreted as a measure of "integrated, crude, ambient energy" and is the amount of water that evaporates from a saturated surface, closely related to latitude and the variability in solar radiation. But whereas much of the solar energy is redistributed by reflection, counterradiation and advection of air and water masses, PET and temperature integrate the re- gional energy balance. (Temperature during the active months of the species considered, used by Turner et al. 1987, in contrast to mean annual temperature used by Currie, may be a better predictor in view of the fact that most species are active only during certain months and would not be affected by lower temperatures during the less active period.)

Currie interprets his findings for vertebrates as mean- ing that species richness is somehow limited by the energy supply in the environment, i.e. ectotherms ab- sorb heat for temperature regulation, and homeotherms use less metabolic energy at increased ambient temper- atures, and/or warmer environments possibly "offer en- ergy sources (niches?) unrelated to local primary pro- ductivity". However, as pointed out by Currie himself, there is a logical limitation (or even inconsistency) in this hypothesis: "why doesn't a small number of species monopolize the available energy?"

Gradients in species diversity with altitude and possibly with depth are well correlated with energy (temperature) Decrease in the number of species with decreasing tem- peratures at higher altitudes is as conspicuous as the decrease with latitude (e.g. Brown and Gibson 1983),

although exceptions occur. For example, there is an almost linear relationship between number of bird spe- cies and altitude in New Guinea (Kikkawa and Williams 1971) and between avian syntopy (= number of species using the forest within ? 30 m of each station) and altitude in the Andes, Peru (Terborgh 1977). Reduced species diversity in the deep sea is not so well docu- mented. Sanders (1968, 1969) found more species of benthic bivalves and polychaetes on the continental slopes than on the shallow continental shelf itself, a finding attributed by Abele and Walters (1979) to the different areas at different depth; as much as 99% of the variation in polychaete species numbers was due to the areal extent of the estuary, bay, shelf and deep sea regions of the study area, the Gay Head - Bermuda transect. Rex (1981) also found a peak of diversity for various benthic animal groups at about 2000 m depth and ruled out a species-area effect. However, a rela- tively low species diversity in surface waters could be expected in his study area: the cold New England coast (41-45?N) of eastern North America. Grassle (1991, further references therein) suggested that diversity of deep-sea benthos is of the same order as in shallow water tropical communities. However, studies of only few areas and taxa (mainly polychaetes and some crus- taceans) have been made, and little is known about the geographical distribution of deep-sea species. In view of the large area of the deep sea (3 x 108 km2 at > 1000 m depth, worldwide), much larger than any surface area of comparable uniformity, a very significant species-area relationship may be expected. Such a relationship, per- haps jointly with the long undisturbed history of the deep-sea (Sanders 1969), could at least partly be re- sponsible for a great diversity. In a comparative study of habitats of similar size in surface and deep waters, that by Rohde (1988) of Monogenea on the gills of teleost fish off southeastern Australia, species diversity was six times greater in temperate surface than in deep waters (Table 5). It should also be emphasized that quantitative data on overall species richness on coral reefs and in mangrove and other tropical coastal habitats are not available because of the simple fact that species counts in such tropical surface waters are practically impossible because of the extreme diversity.

Thus, considering all the evidence jointly, it appears

522 OIKOS 65:3 (1992)

20 - there must be an upper limit to species numbers set by ._.^~~5?~~~~ ~the space on earth available, the minimum physical size

10- / . of organisms and the minimum population size possible, " *" " " * '. ? ?the potential number of niches is almost infinite. Rohde

00 20.0 * 60"80"- (1991) has shown that - at least for parasites, which 0 20 40 60 8'0 represent the majority of animal species - many vacant

niches remain, and Walker and Valentine (1984) sug- 30- . gested that the mean proportion of empty niches for

eight marine invertebrate groups is in the range of 20- \ 12-54% (see also Simberloff 1981). Compton et al.

/ystd

t h

\.. if e(1989) concluded that "conspicuous vacant niches... are 10- easily identified in the South African communities" of

bracken-feeding arthropods. Even if some habitats 0- . . should be filled to capacity, the possibility cannot be

0 ~ 200~ 40 6 0o 8 ?0 ruled out that more species can evolve by subdivision of Time Since Family Origin (years x 106) niches (e.g. Brown and Gibson 1983: the carrying ca-

pacity increases with time due to increasing efficiency of 9. Modified survivorship curves for living mammal families indivi varm (central-west Africa) (top) and cold (northern Eu-

a) regions (bottom). Modified from Stehli et al. (1969). can make a living and pack into communities). The difficulties encountered when trying to explain

greater species richness in energy-rich environments by t correlation between temperature and species rich- higher limits to species numbers, disappear when en- s is as distinct along altitudinal transects as it is along ergy (and particularly temperature) is not related to tudinal ones, but that more studies are needed to species numbers but to evolutionary speed. Differences iblish such a correlation for the depth gradient. in evolutionary speed at different latitudes have been

implicitly or explicitly assumed by several authors, (e.g. Rensch 1954, 1959, Pielou 1979, further references therein). There is a considerable body of data that in-

lergy levels (temperatures) do not dicates higher evolutionary rates in the tropics (Figs 9 termine species numbers but and 10). For example, tropical genera of benthic Fora-

olutionary speed minifera and extant bivalves tend to be younger than high-latitude ones (references in Pielou 1979), and

the last two sections, I have shown that energy (mea- Stehli et al. (1969) found latitude-dependent differences ed for instance by potential evapotranspiration, solar in the rate of evolution in clams, mammals, Permian iation or temperature) correlates well with species brachiopods, and Cretaceous planktonic Foraminifera.

diversity along latitudinal and altitudinal gradients. A possible interpretation could be the assumption that species richness is limited by energy supply (Currie 1991, see above). However, even if higher energy levels result in greater productivity, they do not necessarily lead to greater species numbers (see above). The hy- pothesis that species richness is limited by energy supply (i.e. that different energy levels set different upper bounds on diversity at different latitudes) assumes that habitats are saturated with species, but in spite of fre- quent statements to the contrary, there is little evidence in support of such an assumption. Pianka (1966), citing Elton and MacArthur, stated "there is reasonable evi- dence that the majority of habitats are ecologically sat- urated", but Rohde (1978a, also 1979, 1980a) argued that it may be logically impossible to "prove" that a habitat has as many species as it can support, especially because newly evolved species create new adaptive op- portunities for more species, such as parasites and sym- bionts. Thus, the enormous variety of arthropods in tropical rainforest canopies recently discovered (Erwin 1982, Stork 1988) represents niches for an even greater number of parasites, hyperparasites, etc. Although

90 -

85 -

E, E

a) c0 C

a)

80 - .

* 75 -

* U

70 - .

65 -

.

60 .1

10

.

20 30 40 50

Latitude (?N)

Fig. 10. Mean age of 13 living bivalve faunas of the North American east coast. Mean age of fauna = mean of the ages (million years) of the oldest known fossils of the genera in the fauna. Modified from Pielou (1979) acc. to Hecht and Agan.

34* OIKOS 65:3 (1992)

0o -

a)

LL

ct E E

tc

-j

._

._

Fig. of v rasi;

thal nes latil est<

En del ev( In t surn rad

523

Greater evolutionary speed in the tropics is due to shorter generation times, higher mutation rates, and acceleration of selection Rohde (1978a) has discussed the factors that may be responsible for a greater evolutionary speed at low lat- itudes. They include (1) shorter generation time of many (but not all) poikilothermic and homiothermic animals in the tropics (e.g. Rensch 1954), (2) an in- crease in mutation rates at higher temperatures (refer- ences in Rohde 1978a) and (3) an acceleration of selec- tion leading to fixation of favourable mutants in pop- ulations as a result of the above two points and the generally faster physiological processes at higher tem- peratures.

Concerning the first point, Andrewartha and Birch (1954) and Andrewartha (1971) discussed effects of temperature on speed of development, and Fischer (1960) gave some examples of rapid evolution due to shortness of generation, i.e. development of insecticide resistance in insects and of pathogenicity in bacteria, and of much faster maturation rates of some insects and marine invertebrates at higher temperatures. However his discussion shows that shorter generation times do not always lead to faster evolution (slow evolution in short-generation opossums, fast evolution in long-gen- eration elephants), and that many species are "temper- ature-adapted", i.e. show no significant correlation be- tween temperature and generation lengths. Rosenheim and Tabashnik (1991) have recently shown that there is no theoretical foundation for a linear relationship be- tween generations per year and evolution of pesticide resistance in arthropod pests, a conclusion supported by the examination of data on resistance evolution, gener- ation time and various other biological parameters for 682 North American pests. The authors concluded that generation time can influence evolution of resistance, but does not act in a simple manner. Rather "generation time interacts with a variety of genetic, ecological and operational factors to produce a multitude of effects". It also has to be considered that many tropical organisms do not reproduce continuously. Nevertheless, overall, the number of generations per year in poikilotherms, and to some extent also in homiotherms, is greater at low than at high latitudes (Rensch 1954), and this must have a significant effect on the effectiveness of selection at different latitudes.

Concerning the second point, Rohde (1978a) gave some examples (see also Precht 1955), and temper- ature-dependance of mutation rates has been known since the early studies of Muller. Timof6eff-Ressovsky et al. (1935) found a Qlo of approximately 2.5 for the mutation rate of sex linked lethal factors in Drosophila melanogaster, and a Qlo of approximately 5, if the accel- erated development at higher temperatures was taken into consideration, i.e. the mutation rate follows van T'

Hoff's rule. In Escherichia coli, natural mutation rate has a temperature characteristic similar to growth rate, i.e. the mutation rate per mutable unit per generation is the same at all growth temperatures. In other words, it is greater at higher temperatures because of shorter generation times (reference in Precht et al. 1973). Very high temperatures, i.e. above growth temperatures, have a mutagenic effect in microorganisms and meta- zoans (reference in Precht et al. 1973; see also Ratner and Vasilyeva 1989 for temperature induced mutations in Drosophila). Hoffmann and Parsons (1991) referred to studies of temperature effects on recombination in various eukaryotes and concluded that there is suggest- ive evidence for higher recombination rates at temper- ature extremes, although generalizations are difficult (review in Parsons 1988). Stehli et al. (1969), on the basis of their finding that homiothermic mammals also show faster evolutionary rates in the tropics, doubted that higher mutation rates are responsible for faster evolution. However, exposure to irradiation (including that by light) is known to cause mutations in mammals, and also - as pointed out by Rohde 1978a - it may well be that mammalian diversity is entirely determined by the diversity of plants and poikilothermic animals fur- ther down in the hierarchy.

Concerning the third point, the general acceleration of physiological processes with temperature (within cer- tain ranges), in addition to the faster mutation rates and shorter generation times, must have significant effects on the speed of selection, but I do not know of a single experimental study specifically aimed at determining the effects of temperature on the speed of selection. There is no reference to relevant studies in standard texts, such as Drake (1970), Precht et al. (1973), Dobz- hansky et al. (1977), Parsons (1983), Wohrmann and Loeschke (1984), Calow (1987), de Jong (1988), Font- devilla (1989), and Maynard Smith and Vida (1990), and a search of many recent publications was also nega- tive. Such studies are urgently needed and one main aim of this review is to draw attention to this need.

Conclusion This review has shown that an "ecological", equilibrium explanation of latitudinal gradients in species diversity cannot be given. Although many factors are likely to be responsible for local differences in diversity and for secondary effects on latitudinal gradients, the primary cause appears to be effects of solar radiation (temper- ature) on evolutionary speed. The widespread view that diversity is limited by some environmental factor is based on the unsupported belief that all habitats are filled to capacity. However, saturation of habitats does not rule out a further increase in species numbers by subdivision of niches, and evidence is mounting that many vacant niches exist, particularly for parasites and

OIKOS 65:3 (1992) 524

symbionts. Evolution is gradually filling these niches as the result of greater speciation than extinction rates, (e.g. Hoffman 1990), and greater "effective" evolution- ary time in the tropics because of greater evolutionary speed has led to greater species numbers in the tropics. It is likely that habitats at all latitudes could support more species than presently in existence (and perhaps equal numbers at all latitudes).

Paradoxically, the tropics have more extant vacant niches than colder regions, because the greater number of free-living species provides more opportunities for "dependent" species, such as parasites. Efforts to find

equilibrium explanations for the gradients have led to numerous ecological studies on factors influencing spe- cies diversity, whereas direct temperature effects on

evolutionary speed have been largely neglected. Ur- gently needed are experimental studies on the effects of

temperature on mutation rates and especially on speed of selection.

Acknowledgements - Financial support was given by the Aus- tralian Research Council and the Univ. of New England. M. Heap helped in redrawing some of the figures, N. Watson, C. Nadolny, S. Cairns, and M. Ramsey critically read and B. Rochester typed the manuscript. K. Lim advised me on Alek- seev's paper.

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