Len N. Gillman

THE INFLUENCE OF PRODUCTIVITY ON THE SPECIES RICHNESS OF PLANTS: A CRITICAL ASSESSMENT

Despite much scrutiny the relationship between productivity and species richness remains controversial, and there is little agreement about causal processes. We present the results of a survey of 159 productivity-plant species richness (P-PSR) relationships from 131 published studies. We critically assessed each study with respect to experimental design and for the appropriateness of the surrogates used for productivity. We were able to accept only 60 of the reported relationships as robust tests of the P-PSR relationship and a further 18 as robust tests of the biomass species richness relationship. Previous analyses have found that unimodal P-PSR relationships predominate. In contrast, we found that, in studies that used data of continental to global extent, all P-PSR relationships were positive regardless of grain, that almost all were also positive in data sets of regional extent, and that unimodal relationships were not dominant even in studies of fine grain or small spatial extent. Our results differ substantially from previous meta-analyses because previous studies have included a large number of studies that do not meet basic experimental design criteria for objectively testing P-PSR relationships. These results have important implications for theory that attempts to explain species richness patterns. We critically review four dominant theories in light of our results and develop new falsifiable predictions of relationship from these theories at both small and large spatial scales.

The road from Santa Rosalia: A faster tempo of evolution in tropical climates

Using an appropriately designed and replicated study of a latitudinal influence on rates of evolution, we test the prediction by K. Rohde [(1992) Oikos 65, 514–527] that the tempo of molecular evolution in the tropics is greater than at higher latitudes. Consistent with this prediction we found tropical plant species had more than twice the rate of molecular evolution as closely related temperate congeners. Rohde’s climate-speciation hypothesis constitutes one explanation for the cause of that relationship. This hypothesis suggests that mutagenesis occurs more frequently as productivity and metabolic rates increase toward the equator. More rapid mutagenesis was then proposed as the mechanism that increases evolutionary tempo and rates of speciation. A second possible explanation is that faster rates of molecular evolution result from higher tropical speciation rates [e.g., Bromham, L. & Cardillo, M. (2003) J. Evol. Biol. 16, 200–207]. However, we found the relationship continued to hold for genera with the same number of, or more, species in temperate latitudes. This finding suggests that greater rates of speciation in the tropics do not cause higher rates of molecular evolution. A third explanation is that more rapid genetic drift might have occurred in smaller tropical species populations [Stevens, G. C. (1989) Am. Nat. 133, 240–256]. However, we targeted common species to limit the influence of genetic drift, and many of the tropical species we used, despite occurring in abundant populations, had much higher rates of molecular evolution. Nonetheless, this issue is not completely resolved by that precaution and requires further examination.

Latitude, elevation and the tempo of molecular evolution in mammals

Faster rates of microevolution have been recorded for plants and marine foraminifera occupying warmer low latitude environments relative to those occurring at higher latitudes. By contrast, because this rate heterogeneity has been attributed to a relationship between thermal habit and mutagenesis via a body temperature linkage, it has been assumed that microevolution in mammals should not also vary systematically with environmental temperature. However, this assumption has not previously been empirically examined. In this study, we tested for a thermally mediated influence on the tempo of microevolution among mammals using a comprehensive global dataset that included 260 mammal species, from 10 orders and 29 families. In contrast to theoretical predictions, we found that substitution rates in the cytochrome b gene have been substantially faster for species living in warmer latitudes and elevations relative to sister species living in cooler habitats. These results could not be attributed to factors otherwise thought to influence rates of microevolution, such as body mass differentials or genetic drift. Instead, the results indicate that the tempo of microevolution among mammals is either responding directly to the thermal environment or indirectly via an ecological mechanism such as the ‘Red Queen’ effect.

What is the form of the productivity- animal -species -richness relationship? A critical review and meta-analysis

The nature of the relationship between productivity and species richness has remained controversial for at least two decades. Recently authors have favored the suggestion that the form of this relationship is highly variable and scale dependent. However, this conclusion is not universally accepted. Here we present the results of a meta-analysis of animal productivity-species-richness relationships (PSRR) in terrestrial and freshwater ecosystems. Initially, 374 separate cases from 273 published studies were identified as potential tests of the animal PSRR. After critically assessing each study, 115 cases were accepted as robust tests of the relationship, and of these 95 had data available for formal meta-analysis. Contrary to expectation, we found no support for the form of the relationship being scale dependent; positive relationships predominated at all scales (geographical extents and grains). Furthermore, positive relationships were the most common form of the animal PSRR in both terrestrial and freshwater ecosystems and among vertebrates, invertebrates, homeotherms and poikilotherms. Therefore, our results also contrast with previous reviews that suggest no particular form of the PSRR is predominant. We demonstrate that the method used for classifying the form of PSRRs is critical to the result and that previous reviews may have been too liberal toward classifying the form of relationships as unimodal. The tendency for positive relationships between productivity and species richness across diverse animal taxa has important implications for understanding the mechanisms behind the latitudinal gradient in species richness.

SLOWER TEMPO OF MICROEVOLUTION IN ISLAND BIRDS: IMPLICATIONS FOR CONSERVATION BIOLOGY

Whether microevolution on small islands differs from that on larger landmasses is a key question in biology with substantial implications for species conservation. However, due to the difficulties faced in producing adequately replicated samples and in controlling for confounding variables, prior attempts to examine evolutionary questions relating to habitat area and population size have produced equivocal results. Here we show, using experimental design criteria that reduce the potential for such confounding, that bird species on larger landmasses have higher rates of molecular evolution. The study involves a global dataset of 48 independent contrasts for the cytochrome b gene encompassing all possible paired sister species comparisons (from seven orders and 17 families) that were available at the time of dataset assembly. A more rapid evolutionary tempo in larger areas has important ramifications for biodiversity conservation because it indicates a new imperative, beyond that of simply maintaining preexisting genetic diversity, for securing large areas for threatened species. This result suggests that the trend of confining species to limited refugia is likely to be slowing the tempo of microevolution. That effect might constrain the potential for adaptive shifts in response to changing environments such as those associated with global warming.

Response of forest tree seedlings to simulated litterfall damage.

Litterfall is an important cause of seedling mortality in many forests ranging from wet tropical to boreal. However, there is a lack of studies that investigate differences between species in seedling resilience to litterfall damage. We selected seedling pairs of seven tree species and simulated litterfall damage by pinning one of each pair to the ground. The mortality and growth rates varied significantly between species for pinned individuals, but were similar for unpinned seedlings. The mortality of pinned Nestegis cunninghamii and Prumnopitys ferruginea was significantly greater than that of unpinned individuals (P < 0.05). However, contrary to expectations, the growth rates of pinned Hedycarya arborea and Nothofagus menziesii were much greater than for those left unpinned (P < 0.05). In general, seedling resilience to the bending damage differed substantially between species. N. cunninghamii and P. ferruginea suffered high mortalities and did not increase growth rates in response to damage, whereas, H. arborea and N. menziesii suffered few mortalities and regained height quickly. Other study species demonstrated intermediate resilience. This study demonstrates that some species are more likely to survive in high-risk litterfall regimes than are others. Given that litterfall risk can vary greatly between microsites, these results suggest that litterfall can contribute to regeneration niche differentiation.

Biogeography of photoautotrophs in the high polar biome

The global latitudinal gradient in biodiversity weakens in the high polar biome and so an alternative explanation for distribution of Arctic and Antarctic photoautotrophs is required. Here we identify how temporal, microclimate and evolutionary drivers of biogeography are important, rather than the macroclimate features that drive plant diversity patterns elsewhere. High polar ecosystems are biologically unique, with a more central role for bryophytes, lichens and microbial photoautotrophs over that of vascular plants. Constraints on vascular plants arise mainly due to stature and ontogenetic barriers. Conversely non-vascular plant and microbial photoautotroph distribution is correlated with favorable microclimates and the capacity for poikilohydric dormancy. Contemporary distribution also depends on evolutionary history, with adaptive and dispersal traits as well as legacy influencing biogeography. We highlight the relevance of these findings to predicting future impacts on diversity of polar photoautotrophs and to the current status of plants in Arctic and Antarctic conservation policy frameworks.

Evolutionary speed limited by water in arid Australia

The covariation of biodiversity with climate is a fundamental pattern in nature. However, despite the ubiquity of this relationship, a consensus on the ultimate cause remains elusive. The evolutionary speed hypothesis posits direct mechanistic links between ambient temperature, the tempo of micro-evolution and, ultimately, species richness. Previous research has demonstrated faster rates of molecular evolution in warmer climates for a broad range of poikilothermic and homeothermic organisms, in both terrestrial and aquatic environments. In terrestrial systems, species richness increases with both temperature and water availability and the interaction of those terms: productivity. However, the influence of water availability as an independent variable on micro-evolutionary processes has not been examined previously. Here, using methodology that limits the potentially confounding role of cladogenetic and demographic processes, we report, to our knowledge, the first evidence that woody plants living in the arid Australian Outback are evolving more slowly than related species growing at similar latitudes in moist habitats on the mesic continental margins. These results support a modified evolutionary speed explanation for the relationship between the water-energy balance and plant diversity patterns.

Faster evolution of highly conserved DNA in tropical plants

A faster rate of nuclear DNA evolution has recently been found for plants occupying warmer low latitudes relative to those in cooler high latitudes. That earlier study by our research group compared substitution rates within the variable internal transcribed spacer (ITS) region of the ribosomal gene complex amongst 45 congeneric species pairs, each member of which differed in their latitudinal distributions. To determine whether this rate differential might also occur within highly conserved DNA, we sequenced the 18S ribosomal gene in the same 45 pairs of plants. We found that the rate of evolution in 18S was 51% faster in the tropical plant species relative to their temperate sisters and that the substitution rate in 18S correlated positively with that in the more variable ITS. This result, with a gene coding for ribosomal structure, suggests that climatic influences on evolution extend to functionally important regions of the genome.

Physical damage by litterfall to canopy tree seedlings in two temperate New Zealand forests

Abstract. The importance of litterfall as an agent of physical damage and mortality to canopy tree seedlings was investigated in two New Zealand forests: Huapai Scientific Reserve, a warm temperate forest and Pureora Forest Park, a cool temperate forest. 200 natural seedlings within the 10–30 cm height class and 200 artificial seedlings, made from plastic straws and wire, were monitored at 4–6 week intervals over two years in each forest. Litterfall was the cause of a significant proportion of seedling mortality in each forest (11–18%). Seedling growth rates were measured and used to estimate the mortality that a cohort of seedlings may suffer due to litterfall in the time taken to grow through the 10–30 cm height class. Up to 38% mortality due to litterfall may occur to such a cohort at Huapai and up to 29% at Pureora. Although mortality due to litterfall of natural seedlings was similar in both forests, damage at Huapai (7%/yr) was almost 3 × greater than at Pureora (2.5%/yr) (P < 0.001). Artificial seedlings were damaged due to litterfall at almost five times the rate at Huapai (16%/yr) than at Pureora (3%/yr) (P < 0.0001). The rate of damage to artificial seedlings at Pureora is similar to that reported for a Northern Hemisphere temperate forest, however, the rate of damage to artificial seedlings at Huapai is much greater, and of a similar rate to those reported from tropical forests. The evolutionary and ecological implications of the differences between the rates of damage at Huapai and at Pureora, and the mechanisms promoting litterfall damage to seedlings, are discussed.