The Latitudinal Diversity Gradient Hypothesis: the state of knowledge Biogeography Spring 2013, Term Paper

Title: Latitudinal Diversity Gradient Hypothesis, the state of knowledge By Schibon

1. Introduction
Latitudinal gradients in species diversity are generally understood to be increases in the number of species from high (cold-temperate) to low (warm) latitudes (Rohde, 2011). As early as 1807, von Humboldt provided the first formulation for this hypothesis (based on climate) to explain latitudinal gradients of richness (Hawkins 2001) which has remained one of the key questions in Evolutionary Ecology. No single pattern of biodiversity has fascinated ecologists more than the increase of richness toward the Tropics (Pianka 1966; Rohde 1992; Rosenzweig 1995; Gaston and Blackburn 2000). Still, there is an astonishing lack of consensus about the mechanisms leading to this spatial variation in diversity (Hillebrand, 2004). As the search for a primary cause to this latitudinal gradient has been hampered by the increase number of hypotheses (Pianka 1966; Rohde 1992), their interdependence (Currie 1991; Gaston and Blackburn 2000), and the lack of rigorous falsification (Currie et al. 1999), it makes sense to assess the current state of knowledge on this issue. The current paper aims at updating on the current state of knowledge concerning the latitudinal diversity gradient particularly through reviewing the most dominant hypotheses and theories striving to explain global patterns and causes of the extraordinarily high diversity observed in the low latitude as compared to the high latitude regions of the globe. The document is organized as follows: the next section briefly describes the method we used to collect the material of investigation. Section 3 presents a discussion on the dominant theories associated with the LDGH. And section 4 proposes some global considerations on the temporal evolution of the LDGH as well as some concluding remarks 2. Methods
The ASU online Web of knowledge application, v5.10 was used to perform a Web of Science article search on the latitudinal diversity gradient hypothesis spanning from 1978 to 2013. The search strings were “latitudinal gradient,” and “latitudinal gradient hypothesis.” And this search resulted in 674 articles further screened for relevance to the search topic (particularly for the presence of the search string in the title of the returned articles) and for the number of citation times characterizing such articles. This effort was complemented with a search on Google scholar which allows for bridging the information gap between the early 1950s and 1978, a period when research concerning the latitudinal diversity gradient hypothesis, LDGH was equally active. In this context, additional digital libraries such as JSTOR (Journal Storage) were also browsed. This preliminary step provided us with four high-profile and particularly well cited papers (e.g., Romdal et al. 2013; Hillbrand 2004; Willig et al 2003; and Pianka 1966) which made the substance of our discussion on the LGDH. The main paper summarized here is by Hillebrand (2004) as a chronological bridge between the earliest and the latest reviewed articles. 3. Results
Hillebrand, H. (2004) On the generality of the latitudinal diversity gradient. The American Naturalist, 163, 192–211; Summary of the article
This research paper builds on the lack of consensus about the global pattern and causes of latitudinal diversity gradients and addresses issues related to the predominance of single-gradient/habitat, single-biological group-based and single-region-restricted studies characterizing the latitudinal diversity gradient debate and which “counteracts its associated notion of generality” (Hillebrand 2004). The main objective here was to generate more and stronger knowledge on how ecological and evolutionary features of the organisms, geographic positions, and habitat characteristics change the structure of the latitudinal diversity gradient.
Through associating the difficulty to elucidate the causes and patterns underlying the latitudinal diversity gradient to the existence of too many interdependent and hard to falsify hypotheses, the author provides background and context to his research, through a brief survey of the literature showing the progressive status of the theories and/or hypotheses used to analyze and test the latitudinal diversity gradient hypothesis, LDGH. This review exposed four big mechanisms / hypotheses among those proposed to explain the causes and patterns of increasing diversity at low latitude regions; each of which failed to ultimately bring a flawless support to the LDGH: 1) Changes in the intensity or specificity of biotic interactions with latitude were proposed (by Pianka 1966) as ultimate causes of increasing diversity at low latitudes. But such hypothesis was undermined by several recent contributions (Lambers et al. 2002; Ollerton & Cranmer 2002) which failed to observe consistent changes in interactions across latitudes. 2) Mid-domain models (Colwell and Hurtt 1994; Colwell and Lees 2000) use random placement of species ranges geometrically constrained in a domain (Earth) with hard boundaries (the poles) to predict a peak in diversity in the middle of this domain (the Equator) without invoking any ecological or evolutionary processes. In spite of some relative success associated with high predictive power at global (e.g. Lyons and Willig 1997; Jetz and Rahbek 2001; Koleff and Gaston 2001) and regional scales (e.g. Lees et al. 1999), such models failed in most instances (e.g; Bokma et al. 2001; Diniz et al. 2002) to adequately predict latitudinal gradient diversity. 3) Gradients of decreasing biome area (Rosenzweig 1995) and of energy (and water) supply (Currie 1991; Allen et al. 2002) toward the poles have been hypothesized as ultimate causes for the latitudinal diversity decline. But the relative importance and possible interactions of these covariates (Currie 1991; Rohde 1997; Rosenzweig and Sandlin 1997) are subject to controversy. 4) The effective evolutionary time hypothesis (Rohde 1992) assumes higher speciation in the Tropics as a major cause of the latitudinal diversity gradient. Higher speciation means higher habitat diversification due to the local occurrence of higher energy which increases mutation rates while decreasing generation times (Cardillo 1999). Larger continuous spatial extent of the Tropics favors increased speciation (Losos and Schluter, 2000), with an occurring higher temporal stability on geological time scales which enhances clade persistence (Jansson and Dynesius 2002). In such a formulation, the time hypothesis is a nested set of hypotheses which integrate several of the relevant theories proposed in the 1960s particularly by Pianka (1966). Support to these major hypotheses was biased by their limited selection of organisms (Rohde 1992; Hillebrand & Azovsky 2001) (often one or a few groups surveyed) weakening knowledge of how ecological and evolutionary features of the organisms, geographic positions, and habitat characteristics change the structure of the latitudinal gradient. Such situation motivated the author to test about 600 latitudinal gradients assembled from the literature for (significant) variations in the gradient between organisms, habitats, or regions. Meta-analysis, a method contrasting results from different studies in the hope of identifying patterns among study results fits to latitudinal gradient analysis across different biota and regions and allows generalizing findings on the latitudinal distribution of species richness (Gurevitch & Hedges 1993; Rosenberg et al. 2000). It was used in this study to contribute more generality and universality to studies trying to explain the LDGH historically limited in their biological basis (only one group or a limited number of groups of organisms) and their spatial scale (one continent: the Americas). Ultimately, the author used the collected latitudinal gradients to test if the relation between diversity and latitude varied significantly across the database, with the characteristics of the measurement; the characteristics of the organisms; the scale of observation, and with the habitat types (terrestrial versus freshwater or marine realms). The author found the latitudinal decline of diversity to globally be “a ubiquitous phenomenon, and a highly general pattern across all organisms and habitat types”. Moreover, the magnitude of relations between diversity and latitude was found to be dependent on scale of observation (higher significance at regional than local scales), and on some eco-physiological factors describing the organism (e.g., body mass, trophic level, dispersal type). However, the gradient parameter showed no difference between ectotherm and homeoterm / [endotherm]1 organisms. The range of latitudes covered showed no effect on the structure of the latitudinal gradient whereas the grain (spatial resolution) of the study influenced the relation between diversity and latitude particularly with large sampling areas. The latitudinal gradient was also found to vary significantly with longitude (i.e., between continents or oceans).
1 The author contrasted ectotherm and homeotherm in the article. But, normally ectotherm should have been contrasted with endotherm.
Clearly most hypotheses proposed (in the past) as possible explanations to the latitudinal diversity gradient turned out to be either weakened or falsified by the Hillebrand 2004 study’s outcome. For instance, the larger extent area hypothesis proposed by many authors to support the LDGH was not supported by this study as diversity gradients on the Northern Hemisphere are neither stronger nor steeper than on the Southern Hemisphere. And although the global distribution of area, and spatial heterogeneity were found to vary with latitude by Gaston and Blackburn (2000), it remains unclear if they work individually (Rohde 1992) or synergistically (Gaston and Blackburn 2000) as primary causes of latitudinal diversity. Latitudinal diversity gradients in freshwater were weaker and flatter than their terrestrial or marine counterparts. In contrast, marine gradients were found as strong or even slightly stronger as compared to terrestrial gradients. The marine gradients also showed substantial variations between habitats, with strong gradients in the pelagic ocean and in the deep sea. Such strong gradients negate all support to the LDGH. Crucial enough, within the terrestrial realm, highly complex forest habitats did not show gradients differing from grasslands, wetland, or other less structured habitats. Finally, and as Zapata et al. (2005) the author found the mid-domain models to fairly support the LDGH. The global results from Hillebrand (2004) test several additional hypotheses and theories proposed to explain the latitudinal diversity gradient. Some of which are supported through the author’s article either alone or in combination with other factors. In this setting, an interaction of energy and area-related processes is supported because many significant factors relate to differences in energy acquisition and processing (body mass, trophic level) or in area (habitats) or both (continents). As the Hillebrand’s 2004 provides only a partial account of the many theories and/or hypotheses accounting for the increasing species diversity toward low latitudes, respective pieces from Pianka (1966), Rhode (1992) and/or Willig et al. (2003) were reviewed for the purpose of complementing the literature on the LDGH and get a better perspective on the Hillebrand’s paper. Pianka (1966) proposed a more exhaustive listing of hypotheses which he discussed succinctly within a context of novelty, substantial lack of ecological data, and absence of an adequate conceptual framework (e.g.; at the time of the Pianka’s article publication, an official definition of diversity was yet to exist). Through reviewing the diversity indices in vigor at the time and underlining the absence of consensus characterizing the debate surrounding the LDGH (a trend still dominant in today’s literature), Pianka (1966) queried the factors allowing ecological co-existence of more species at low latitudes. Such factors were found to be distributed in six more or less distinct hypotheses: the time theory, the theory of spatial heterogeneity, the competition hypothesis, the predation hypothesis, the theory of climatic stability, and the productivity hypothesis. Those hypotheses very simple in formulation refer to single explanatory factors for the latitudinal gradient diversity, a trend which has historically characterized the field. They have served as input for the subsequent formulations, more sophisticated in nature. They are briefly double-checked with the Hillebrand 2004’s review list and further evaluated for their respective performance in supporting the LDGH. The time hypothesis assumes that older communities are more diverse. This hypothesis, which cannot be tested directly (Willig et al. 2003), assumes ecological forms involving ecological disturbance and local dispersal (Rohde 1992), and evolutionary forms entailing geological perturbation and speciation or extinction. It is not clearly mentioned by Hillebrand 2004. The spatial heterogeneity theme assumes an inverse relationship between latitude and environmental complexity. Nonetheless, no general gradient in heterogeneity has been demonstrated (Rohde 1992). And highly complex forest habitats did not show gradients differing from grasslands, wetland, or other less structured habitats (Hillebrand 2004). The competition hypothesis assumes that increased competition may lead to more species per unit habitat space, or predation may reduce prey population levels, thereby allowing more prey species to coexist in the tropics (Pianka 1966). Interspecific interactions may [indeed] be costlier at lower latitudes where, for example, organisms invest more energy or resources in combating parasitism (Møller 1998). The predation hypothesis assumes comparatively lower competition between prey population in the Tropics as a result of the top-down control exerted by numerous predators (and/or parasites). Ecological interactions such as competition or predation clearly can regulate local diversity (Huston 1999; Shurin et al. 2000; Worm et al. 2002), but the importance for the latitudinal gradient has to be questioned as a consistent change in ecological interactions with latitude was not found and large-scale diversity patterns are not due to variations in community richness (Collins et al. 2002; Stevens and Willig 2002, Hillebrand 2004). The theory of climatic stability posits latitudinal diversity gradient as a result of species specializing into narrower and narrower niches in response to more stable climate conditions, prevailing in the tropics as compared to the high latitudes. The high latitudes are the object of more changeable climate conditions. Nevertheless, Rohde (1992) negates the evidence that abiotic rarefaction differs between high and low latitudes. The productivity hypothesis speculates that: the annual input of solar radiation determines energy availability, productivity, and biomass, and is inversely related to latitude (Robinson 1966). Some measures of productivity generally are correlated to species richness, but not in all organisms as evidenced by Curry (1991). It fails to elucidate how or why species richness increase to a maximum set by energy availability and some studies (e.g., MacArthur 1972) show species richness both as an increasing and decreasing function of high (ecosystem) productivity so that: productivity alone cannot explain latitudinal gradients of richness (Willig et al. 2003) Furthermore, productivity is not consistently correlated with species diversity. It is low, for example, in some tropical seas with high diversity (Rohde 1992). The evolutionary rate theme has been invoked to produce latitudinal gradients of richness (Rosenzweig 1975). For example, high speciation rates have been linked to the great richness of the lowland wet tropics (Brown 1988). Other mechanisms (such as the larger area, increased productivity, and greater environmental predictability) have been invoked as causes for these purported high speciation rates and low extinction rates in the tropics (Rosenzweig 1975). From a methodological perspective, the accurate measurement of rates is a challenge in the evaluation of these hypotheses (Brown 1988). Furthermore, the body mass impact observed by Hillebrand (2004) might indicate the importance of dispersal limitation for the maintenance of the diversity gradient. Despite Hillebrand’s (2004) modest promise that his “results do not serve to directly falsify or support the models proposed to explain the latitudinal diversity”, it turned out that several long-standing hypotheses along with their eventual associated models are found to be properly undermined through his article. This is the case for the time theory, the theory of spatial heterogeneity, and the competition hypothesis. In fact, among the six theories / hypotheses reviewed by Pianka (1966) to explain the latitudinal diversity gradient, only the climatic stability theory and that of productivity were not challenged and eventually falsified by Hillebrand (2004). Willig et al. (2003) complement and improve the literature on the LDGH through an again more exhaustive review of themes and hypotheses accounting for the latitudinal decline in species diversity. The related paper discusses some previous contributions (e.g., Pianka 1966, Rohde 1992) and list no less than 30 hypotheses some of which are modern sophistication of the basic formulations by Pianka (1966). New threads or formulations listed by Willig et al. (2003) include: 1) The Geographic Area Hypothesis (Rosenzweig 1995) postulates that a larger spatial extent supports high diversity and interacts with elevated productivity to produce a gradient of increasing richness toward low latitude regions (Willig et al. 2009). It received both supporting (e.g.; from Ruggiero 1999; Rosenzweig 1995) and undermining (e.g., from Rohde 1997; Kaufman & Willig, 1998) reactions which make it a very controversial rather than a universally agreed-upon theory. 2) The Ambient Energy Hypothesis is an umbrella hypothesis under which other minor hypotheses (e.g.; climatic stability, environmental stability, environmental predictability, seasonality, and harshness) are subsumed. It assumes that environments at high latitudes have mean conditions farther from organismal optima than do their low-latitude counterparts. Research works from Turner et al. (1987), and from Currie (1991), and Currie & Paquin (1987) strongly supported the LDGH.
3) The Rapoport-Rescue Hypothesis is derived from the Rapoport's rule, a pattern in which the size of the distributional ranges of species is related inversely to latitude (Rapoport 1975, Stevens 1989). It holds that species richness is augmented by the addition of “accidentals,” species that normally would not persist but are “rescued” by continual dispersal from nearby favorable areas. Many taxa exhibit both latitudinal gradient of richness and Rapoport's rule in parallel. Such statement supports the mentioned hypothesis as an explanatory mechanism to the latitudinal diversity gradient.
4) The Evolutionary Speed Hypothesis (Rohde 1992) assumes an increase of diversity toward the low latitudes as a function of temperature-induced increases in rates of speciation. Jablonski (1993) suggested the tropics to have been a source of evolutionary novelty throughout geologic time as evidenced by higher origination rates of post-Paleozoic marine orders in equatorial areas compared to temperate areas. However, a recent quantitative analysis provided no support for that theory (Bromham & Cardillo 2003).
Whereas ecological explanations for the latitudinal diversity gradient have dominated the literature in the past 20 years (Wiens & Graham 2005), evolutionary mechanisms are now gaining momentum (Hawkins et al., 2006; Mittelbach et al., 2007; Ricklefs, 2007; Araújo et al., 2008). Despite lack of consensus on the issue, some evolutionary ecologists including Brown & Lomolino 1998, Farrell et al. 1992, Futuyma 1998, Ricklefs & Schluter 1993 happened to converge on a unified explanation for the latitudinal diversity gradient through the niche conservatism hypothesis a.k.a tropical conservatism hypothesis (Wiens & Donoghue 2004). This hypothesis posits that species distribution patterns are governed by ancestral climatic affinities (Romdal et al. 2013). Romdal et al. (2013) use similar methods as Hillbrand (2004) (e.g.; meta-analysis) to test if a prediction derived from this hypothesis is met by analyzing the slope of latitudinal diversity gradients derived from 343 studies from around the world under a timeline of global climatic variation for the past 750 million years. They found that latitudinal gradients of diversity between clades originating in different climate categories were significantly different from each other with clades originating during relatively cold climatic periods exhibiting weak to nonexistent present-day latitudinal gradients in clade richness. Clades originating during ‘transitional/warm’ periods have steep latitudinal gradients, although clades originating in the warmest periods have a relative shallower latitudinal gradient. Their results support the idea that current diversity gradients carry the footprint of historical climates, and posit niche conservatism as a major mechanism involved in generating the current diversity gradient. Higher diversities have arisen among tropical clades because the earth has been predominantly tropical throughout most of its history. 4. Conclusions and future directions
From the above presented discussion, it is clear that the debate related to the latitudinal diversity gradient has generated a number of hypotheses/mechanisms and/or theories attempting to explain the latitudinal diversity gradient. Such debate is bound to perpetuate for long time eventually becoming more and more heated as none existing single theory or hypothesis suffices in itself to adequately explain the latitudinal diversity gradient. Most theories herein reviewed appear to be: overly specific, redundant, and interlinked. It seems that species diversity is ultimately controlled by a combination of factors. Efforts towards elucidating the causes and patterns of the latitudinal diversity gradient should be (more efficiently) spent in the accrued integration/combination of individual factors known to have an influence on that parameter. In fact, if multiple factors interact to cause the latitudinal gradient of richness, it is doubtful that the evaluation of these factors in isolation will bring about meaningful progress (Rosenzweig 1975, Willig 2001). As most tested hypotheses taken in isolation fail badly to explain the latitudinal gradient, it seems that the way forward in solving the “mystery” of the latitudinal diversity gradient lies in the merging and combination of individual mechanisms/hypotheses/theories known to partially explain the latitudinal gradient. Our suggestions are to encourage meta-analysis based studies further supported by Multi-Criteria Decision schemes / tools allowing for assessing the relative contribution of each participating mechanism to the final result with the option of dropping the mechanisms with low or none explanatory power.
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