AWA: Academic Writing at Auckland

Abstract

Gymnosperms were once the dominant feature of the world’s forests, but since the rise of the angiosperms in the Cretaceous they have seen a rapid decline in the lower temperate and tropical regions. This change in spermatophyte distribution as evident in the fossil record has brought about many questions regarding forest dynamics and why angiosperms were so ‘superior’ to their gymnosperm competitors. There have been many theories put forth to explain this phenomenon looking at biotic interactions, relative growth rates, nutrient economy, species evolution and climate change. None have been able to definitively explain gymnosperm dynamics and what caused the decline in their dominance, but what is evident is that gymnosperms species are managing to persist in the environment by utilising the spaces where angiosperms are unable to compete.

Key words: angiosperm, biotic interaction, climate, competition, cretaceous, evolutionary radiation, gymnosperm.

Introduction

There are a multitude of growth and reproductive strategies used by the plant kingdom in order to survive and propagate. Some strategies have been more successful than others, but often this is not uniform across all ecosystems and divides have formed and persisted over the millions of years of evolution creating the mosaic of species traits we see today. It is still not fully understood how some seemingly ‘inferior’ traits have survived in the light of more competitive strategies, one such divide that will be the focus of this review is between that of the gymnosperms and angiosperms. Gymnosperms are a monophyletic group containing the oldest tree forms still living today, argued to date as far back as the Devonian period (419.2-358.9mya) (Chamberlain, 1935; Chaw, Parkinson, Cheng, Vincent, & Palmer, 2000). They comprise a group of plants that produce seeds unprotected by an ovary or fruit (Chaw et al., 2000). The largest group of gymnosperms are the conifers e.g. pines, followed by cycads, gnetophytes, and ginkoales (Chaw et al., 2000). Angiosperms are the most diverse group of land plants that diverged from gymnosperms sometime around the Triassic period (245-202mya) (Doyle & Donoghue, 1986). Angiosperms reproduce via seed production as well, and are differentiated from gymnosperms by the development of flowering organs, endosperms within their seeds, and fruits encasing their seeds(Doyle & Donoghue, 1986).

Angiosperms underwent a rapid radiation during the cretaceous period when we see the first evidence of flowering organs (Doyle & Donoghue, 1986). During this period angiosperms quickly outcompete the well-established gymnosperms as the dominant tree type in the canopy of most tropical and temperate forests, and have held this dominance ever since (Doyle & Donoghue, 1986). However, despite this pattern gymnosperms have managed to persist and still outcompete angiosperms in some ecosystems, particularly in the cooler more nutrient poor regions at higher latitudes and altitudes, and this is prevalent throughout the fossil record (Bond, 1989).

This review will focus on the relationships between gymnosperms and angiosperms and critically analyse some of the ideas put forward to explain the patterns in distribution that we see today. We will seek to answer the question “how gymnosperms have managed to persist in the face of their ‘superior’ angiosperm competitors?” by looking at some of the traits of modern gymnosperms and how they have aided gymnosperm survival. There have been many theories put forward to explain these phenomena and hey can be categorized into five general frameworks that will be discussed. These include an ecological framework, a carbon framework, a nutrient framework, a climate framework and a diversification framework (Augusto, Davies, Delzon, & De Schrijver, 2014).

An ecological framework

The ecological framework attributes angiosperm radiation to the development of traits that allowed them to take advantage of biotic interactions (Augusto et al., 2014). A major theory for the expansion of angiosperms is attributed to their reproductive strategies and mutualist relationship with insects that developed from the evolution of flowers. One theory developed by Regal (1982) looked at pollination strategies and gene flow in populations. Nearly all gymnosperms are wind pollinated which puts them at a disadvantage to insect pollinated angiosperms for two reasons, the first is insect pollination is more specific meaning less energy needs to be spent on pollen production, and second, insect pollination leads to better (more specific) cross pollination between populations especially in more sparsely distributed plant communities (Regal, 1982). Regal (1982) argued that gymnosperms that rely on wind pollination are only advantaged when they exist in monospecific stands because this allows better mate crossing. These stands also happened to occur more often in stressed environments because only a few species are capable of surviving in stressed areas and thus this allows large propagations of one or a few species to develop. This is why we get patterns of larger gymnosperm population formation in environments such as the expansive coniferous forests of the Taiga in the Arctic Circle.

This model promotes the idea that angiosperms have better gene flow due to biotic relationships making them fitter. A current example of this can be seen in red spruce (Picea rubens) which has been declining over the past 100 years, creating sparse populations with low gene flow and inbreeding depression(Rajora, Mosseler, & Major, 2000). In the smallest of populations inbreeding is at its highest and signs of inbreeding depression are more frequent, while the larger populations are maintaining more genetic diversity indicating that this species struggles to cope when population numbers decrease below a certain threshold (Rajora et al., 2000). However there are difficulties with this theory. There is little evidence to suggest that wind pollination is actually inferior to insect pollination (Ellstrand, 1992). In fact a study on a range of Leucadendron spp. (angiosperms) in South Africa showed that wind mediated pollen transfer was just as effective at achieving pollination as insects in this genus and that these were both stable evolutionary traits (Welsford, Midgley, & Johnson, 2014). This evidence possess a difficult question in that if wind pollinated gymnosperms dominated the canopy in large numbers to begin with then the wind pollination strategy should in theory be adequate to continue their genetic diversity like it is doing in the larger populations of Red Spruce, so why did we see a decline?

Other theories have looked at the prospect of herbivory influence and the development of vegetation growth strategies utilised by angiosperms and gymnosperms. Coley (1988) put forth the plant anti-herbivore defence model which described angiosperm fast growth rates as a trade-off. Angiosperms have opted for growing faster over producing less palatable leaves that require more energy input. This is in response to herbivory which has also coincidentally made them more competitive against gymnosperms in resource rich environments that have much slower growth rates (Coley, 1988). Angiosperms are able to grow and reproduce at faster rates and thus overtook gymnosperms due to larger population numbers. Unfortunately in light of data obtained from new genetic technologies the relationship between plant secondary metabolites and herbivores is complex and evidence of secondary metabolite expense and its direct link to maximum growth rate reduction is scarce.

A carbon framework

The carbon framework hypothesizes that angiosperm radiation can be attributed to relative growth rates (Augusto et al., 2014). One theory that has been put forward was by Bond (1989) dubbed the ‘slow seedling’ hypothesis. Bond’s (1989) argument was that this apparent limitation on gymnosperm spread was associated not with mate access but with vegetative and reproductive processes. This theory is similar to Coley (1988) in that it states angiosperms have faster foliage production early on in development and spend less energy on creating woody structural support; they also have faster reproductive cycles. These traits contribute significantly to survival in the early seedling stages and allow rapid regeneration for angiosperms that outcompetes gymnosperm regeneration. This leaves gymnosperm seedlings at a disadvantage in most ecosystems as they have low photosynthetic rates in their leaves which prevent them from achieving high productivity until enough leaf mass has accumulated later in the development of the plant (Bond, 1989). Gymnosperm abundance in more marginal climates can be attributed to a lack of seedling competition in these early stages allowing them to propagate. The implications of this hypothesis thus maintain the idea that in their early evolutionary stages, angiosperms invaded the gymnosperm forests and commandeered their regeneration niche causing the retreat of gymnosperms to more marginal climates where rapid regeneration growth is restricted by ecosystem nutrient availability, and cold climate, taking away the angiosperms competitive advantage.

The basis of this model lies on the assumption that gymnosperms are inherently slower growers relative to angiosperms in high productivity environments; however this may not necessarily be true. Becker (2000) suggested that the transport systems of gymnosperms and angiosperms may be comparable, and that previous measuring techniques looking at leaf venation and xylem conduits are not equivalent descriptors of transport capabilities across different species of spermatophytes. Becker (2000) stated that specialized transfusion tissues in conifer needles may equalize hydraulic conductance’s in leaves equating them to angiosperms. Also, when considering maximum leaf photosynthetic rates mass-based gas exchange rates  are more relevant to seedling competitive ability than the leaf area, which Bond (1989) used (Reich, Walters, Tjoelker, Vanderklein, & Buschena, 1998). We also need to take into account that trait correlation with growth rates can differ across the different life stages of the plant. Leaf area has been found to correlate with seedling growth rate but not adult growth rate(Gibert, Gray, Westoby, Wright, & Falster, 2016). Overall relevant comparative measuring techniques need to be carefully considered when comparing angiosperm and gymnosperm growth rates as these two monophyletic groups diverged so long ago, a lot of adaptive evolution has occurred between them and many different coping mechanisms are utilised to deal with their environment they exist in today. These may appear quite structurally diverse but serve similar purposes that we are missing. Thus it would be more advisable to be measuring relative outputs and molecular exchange rates rather than organelle structural dimensions.

Another flaw in Bond (1989)’s theory was that angiosperm trees selected for the study were all early successional species, meaning Bond’s theory may not be relevant to late successional angiosperms (Becker, 2000). The selection of early successional species would explain any apparent differences in growth rates as faster height growth is beneficial to early succession species in general (Shainsky & Radosevich, 1992). Another key assumption of Bond (1989) is that gymnosperms are restricted to nutrient poor regions. However, these nutrient poor regions may actually be facilitated by gymnosperms. A study looking at plant-soil feedbacks in tropical montane forests found that soil nutrients (inorganic nitrogen, labile phosphorus, and the nitrogen mineralization rate) were more deficient under the canopy of conifer species Dacrydium gracilis than broadleaf species Lithocaprus clementianus (Ushio et al., 2017). This is due to gymnosperms leaves having longer life spans in part from higher lignin content, and lower nitrogen and phosphorus (Cornwell et al., 2008). The study went on further to show that seedlings of the respective species had higher success propagating under the canopy’s of the same species rather than the other (Ushio et al., 2017). This indicates that there is a plant-soil feedback occurring where these two species are creating a favourable soil environment, not a result of the nutrient content of the soils. This also poses more questions as to how angiosperms were able to penetrate this seedling niche when they would have been disadvantaged by the soil nutrient composition created by the existing gymnosperm species.

A nutrient framework

Berendse and Scheffer (2009) theorise that the massive angiosperm shift in vegetation was a result of positive and negative feedback in nutrient cycling between plants and their environment. Angiosperms have higher growth rates which require greater nutrients in their environment. Angiosperms are able to facilitate this nutrient availability by producing litter which is easier to decompose thus releasing more nutrients for their growth (Berendse & Scheffer, 2009). This plant soil feedback allows angiosperms to create fertile environments that benefit their growth over their gymnosperm competitors. Berendse and Scheffer (2009) reason that when angiosperm abundance reached a critical point in the cretaceous period a flood gate effect occurred and angiosperms rapidly assimilate the ecosystem. This theory explains the relatively instantaneous take over in the fossil records during the cretaceous period, despite their origins being traced back to the Triassic period. This also explains why early angiosperm fossil evidence is found to originate in areas of high disturbance, xeric or aquatic habitats and appears to have moved inward toward the gymnosperm stands (Hickey & Doyle, 1977; Mohr & Friis, 2000). Their evidence for this was in the relatively rapid (<10 years) expansion of grass species in heathlands that overtook the ericaceous dwarf shrubs in the area. This was triggered by atmospheric N-inputs after farming was ceased, and accelerated by the effect of the grasses on the soil nutrient release (Berendse, 1998). However there is little other empirical evidence to back up these claims and what data has been recorded has only shown minor changes in nutrient levels indicating that it is unlikely that nutrient levels alone could have caused such a dramatic change (Augusto et al., 2014). This theory also does not go into detail about why we still see such a strong persistence of podocarp species (gymnosperms) thriving within angiosperm dominated forests particularly in the southern hemisphere (Brodribb, Pittermann, & Coomes, 2012).

A diversification framework

The diversification framework looks at the rapid radiation of angiosperms and explains their dominance as a product of their ability to diversify into several new key niches that gave them a competitive advantage (Augusto et al., 2014). Greater phylogenetic branching and evolution rates can be seen in the contrast between angiosperms and gymnosperms, where gymnosperms have maintained a more conserved array of traits and angiosperms have developed more diverse forms and functions (Davies et al., 2004). An answer to why this occurred may be in the molecular evolution of these plants. Despite evidence to show that gymnosperms have undergone evolutionary adaptations during the angiosperm radiation, the molecular data shows their evolution rates to be as much as 7 times slower than angiosperms due to the considerably longer generational times and slower mutation rates(De La Torre, Li, Van de Peer, & Ingvarsson, 2017). Currently it is thought that the reduction in gymnosperm species in response to angiosperm radiation can be attributed to higher extinction rates among the gymnosperms caused by angiosperm competition rather than low levels of speciation among the gymnosperms (Crisp & Cook, 2011).

This model provides some genetic basis and mechanisms for the changes seen in the plant communities however can only really be viewed in collaboration with other theoretical frameworks as the idea of divergence into new niches also requires an understanding of what those niches are and how they aided the species survival and reproduction. This framework covers questions of ‘how’ this change in community structures could have occurred but requires other frameworks to explain the ‘why’ community structures have changed and gymnosperms persisted.

A climate framework

The last framework is the climate framework that looks at the effects of climate and how this has influenced the movements of gymnosperms. It is assumed that climate plays a limiting factor in angiosperm establishment in cooler climates, due to a lack of frost tolerance. This has allowed gymnosperms to seek refuge in these areas. Case studies of modern gymnosperms also appear to show strong relationships with climatic boundaries and it has also been theorised that the reason for the high extinction rates of gymnosperms was a result of changes to dryer climates in the Eocene (Crisp & Cook, 2011).

By far the most successful of all gymnosperms are the conifers and of these Pinaceae that dominate the Northern Hemisphere, so much so that angiosperms struggle to compete in these areas and thus leave niche gaps open for gymnosperms to take advantage of. The highest correlations found in Pinaceae distribution are associated with climatic regions prone to freezing (Brodribb et al., 2012). As a result we find many adaptations to these environments in their species specific growth strategies. Some common features of Pinaceae include high freeze tolerance due to their resistance to freeze-thaw embolism. They have very efficient photosynthetic needle like leaves that can produce maximum photosynthetic rates that are at least on par with, and even greater than associated angiosperm trees (Brodribb & Feild, 2008; Turnbull, Tissue, Griffin, Rogers, & Whitehead, 1998). They also exhibit low wood density which enables a fast volume growth under high light conditions (Becker, 2000). These traits shared by Pinaceae appear to have allowed rapid dispersal across the Northern Hemisphere postglacial landscapes (Brodribb et al., 2012). Other features that we find in these colder zones are slower decomposition and lower nutrient flux in the soils. Pinaceae also contribute to these poor soils by harbouring longer lived leaves meaning there is a lower rate of organic matter joining the leaf litter and thus lower rates of nutrient cycling. On the other side of this adaptation longer lived leaves mean that Pinaceae is utilising more efficient resource use strategies where its leaves are able to generate more photosynthesis over the course of their lifetimes than angiosperm leaves ergo the energy input to growing leaves has a higher payoff (Brodribb et al., 2012).

The climatic framework provides some broad parameters in which we can view spermatophyte evolution and can go some way into explaining the general trends we see in modern plant species and the fossil record. However as we see with many things in nature there are multiple factors that drive evolution. The climatic model can help us understand why there are so many gymnosperms in the higher latitudes and how they have adapted, but do not cover entirely why so many gymnosperms disappeared form the warmer lower latitude areas where they already existed and did not adapt to these changing environments.

Discussion

So far the theories proposed have all taken on a view point of gymnosperms being inferior to angiosperms and that their relative confinement e.g. in northern regions and higher altitudes, is a refugium response whereby they have been excluded from the more favourable areas of the fertile tropics and lowlands and forced into marginal regions. However this notion harbours a very human ideal of what is considered ‘good’ habitat vs a ‘stressful’ one. An alternative to this perspective is to look at the how gymnosperms are taking advantage of environments where angiosperms are not across the globe. Gymnosperms display a range of traits that are advantageous over angiosperms in certain environments. Most literature focuses on the Pinaceae which is the largest and most commercially useful group to humans. However there are many family’s within gymnosperms that have all found their own niches and all of which are managing to thrive.

What we are seeing in colder regions is Pinaceae species that are thriving in harsh climates with low nutrient availability. Not only this, but they are at their highest species diversity and contributing to maintaining these low nutrient environments (Augusto et al., 2015). Angiosperms have adapted some traits to cope with these circumstanced such as deciduousness which allows them to recoup resources and protects from damage during the harshest winter seasons (Augusto et al., 2015). However in the hardest of climates in the far north and highest altitudes deciduousness cannot compete with gymnosperm resilience to the freeze (Brodribb et al., 2012). At the times of angiosperm radiation temperature and humidity at the mid latitudinal zones were at a high and it is thought that perhaps gymnosperms were not particularly competitive at this time as they required these more ‘stressed’ environments to thrive. Therefore angiosperms were advantaged, but Pinaceae adapted by moving to cooler climates better suited for them which is why we see this retreating pattern of the Pinaceae in the cretaceous period (Brodribb et al., 2012).

Podocarps are another diverse family within the gymnosperms that show wide spread distributions across the southern hemisphere and can be found anywhere from sea level to the tree line. They are the most successful gymnosperms in this Hemisphere, although this is still significantly less that what is observed in the dominating Pinaceae of the north. Podocarps have developed different strategies to Pinaceae. They have adapted to survival in more lowland and tropical areas, and they tend to coexist with angiosperm species rather than dominate in monospecific cohorts (Brodribb et al., 2012). Podocarps are very different from Pinaceae in that they are far more drought sensitive and thus would struggle to survive in the type of dry climates Pinaceae do. They have also adapted to angiosperm competition by developing broader flatter leaves that allow more light absorption in shaded areas (Biffin, Brodribb, Hill, Thomas, & Lowe, 2012). These patterns developed during the angiosperm radiation indicating that they were an evolutionary response to the greater shade and water availability created by broad leaved angiosperms (Biffin et al., 2012). Their distribution is limited around the 20° N latitude which is where rainfall tends to drop off and freezing exposure begins (Biffin et al., 2012). This distribution and evolutionary traits show that this family of gymnosperms are capable of maintaining a coexistence with angiosperms and can compete directly with them.

A third family of gymnosperms, the Cupressaceae, display an interesting range of the traits that cover adaptations made by both Pinaceae and Podocarpaceae. This family has a remarkable tolerance for extremes in environmental moisture levels. Some species are swamp dwelling while others are the most water stress resistant species documented (Willson, Manos, & Jackson, 2008). This has allowed them to coexist with both the Podocarpaceae in more cool wet areas and Pinaceae in drier regions in both the Northern and Southern Hemispheres, although the majority of species within this family inhabiting a similar latitudinal zone to the Pinaceae.

In conclusion there are many frameworks in which to explain the apparent patterns in spermatophyte distribution. None have been able to as of yet definitively explain the reason for the reduction in gymnosperms from globally dominant canopy species they once were. There are implications with all the models and it is likely that we will find that it is a combination of factors involving changing climates, life history traits, resource availability and ecological interactions that have all had some part to play in the spermatophyte dynamics. However, even though gymnosperms have undergone large changes since the Eocene they are still persisting and even out-competing the angiosperms in certain ecosystems. Evolution of their structural morphology, transport systems, photosynthesis capabilities and distribution patterns show that gymnosperms have adapted to this new era of angiosperms and are still able to persist by utilising the spaces that angiosperms cannot which is why they are still prominent features in our ecosystems today. Future endeavours to understand this mystery will need to focus on teasing out the relative impacts these theorised frameworks have had on gymnosperm communities and develop a more suitable multidriver hypothesis for gymnosperm evolution. More research needs to focus on the broader group of gymnosperms as a whole, and on the podocarps that have managed to coexist in angiosperm dominated environments if we are to better understand the strategies that have allowed gymnosperms to persist in the forest ecosystems. It is clear from the fossil evidence that something changed with the introduction of angiosperms but we are still far from understanding what the main mechanisms that facilitated this change were. We will perhaps find this answer once we have figured out what factors have allowed the currently surviving species of gymnosperms to avoid extinction.

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