120 years of untangling the divaricate habit: a review - UC Research Repository
←
→
Page content transcription
If your browser does not render page correctly, please read the page content below
Available online at www.science.canterbury.ac.nz/nzns
120 years of untangling the divaricate habit: a review
Kévin J. L. Maurina* & Christopher H. Luskb
a
School of Science, The University of Waikato, Hamilton, New Zealand;
b
Environmental Research Institute, The University of Waikato, Hamilton, New
Zealand
*The University of Waikato – School of Science, Private Bag 3105, Hamilton
3240, New Zealand, kjlm1@students.waikato.ac.nz
(Received August 2020, revised and accepted January 2021)
The evolution of divaricate plants in New Zealand has been the subject of long-
running debate among botanists and ecologists. Hypotheses about this remarkable
case of convergent evolution have focused mainly on two different types of selective
pressures: the Plio-Pleistocene advent of cool, dry climates, or browsing by now-
extinct moa. Here, we review the scientific literature relating to New Zealand
divaricates, and present a list of 81 taxa whose architectures fall on the divaricate
habit spectrum. We recommend a series of standardised terms to facilitate clear
communication about these species. We identify potentially informative areas of
research yet to be explored, such as the genetics underlying the establishment and
control of this habit. We also review work about similar plants overseas, proposing
a list of 53 such species as a first step towards more comprehensive inventories;
these may motivate further studies of the ecology, morphology and evolutionary
history of these overseas plants which could help shed light on the evolution of
their New Zealand counterparts. Finally, we compile published divergence dates
between divaricate species and their non-divaricate relatives, which suggest that
the divaricate habit is fairly recent (< 10 My) in most cases.
Keywords: convergent evolution; divaricating shrubs; heteroblasty; moa; New
Zealand; structural plant defences
Introduction Central Europe, where plants do not show
similar architectures. These plants are
The earliest mention we have found of nowadays recognised as a collection of shrubs
what we call today “divaricating plants” or and early growth stages of heteroblastic trees
“divaricates” was made in 1896 by German bearing small leaves on tangled branches
botanist Ludwig Diels. He described them diverging at wide angles.
as “systematically distant descendants of Such a case of convergent evolution
the New Zealand forest flora that converged naturally attracted much attention from
towards a xerophytic structure” (Diels 1896, local and overseas botanists and ecologists.
pp. 246-247, translated from German). The centre of this attention was to identify
He expressed surprise at seeing apparently putative selective forces that may have
drought-adapted species in climates that driven this evolution. Diels (1896) initially
are generally more humid than in his native proposed drought as the main selective factor,
New Zealand Natural Sciences (2021) 46: © New Zealand Natural SciencesNew Zealand Natural Sciences 46 (2021) 2
and McGlone & Webb (1981) considered Characterising the diversity of
that frost and wind might also have been divaricating habits: variations on a
important. Diels’ climatic hypothesis remained New Zealand theme
largely unchallenged until Greenwood &
Atkinson (1977) developed the moa-browsing
hypothesis that several authors had previously Past attempts at defining the divaricate habit in
hinted at (e.g. Denny 1964; Carlquist 1974; New Zealand
Taylor 1975), igniting a passionate debate
“Divaricate” comes from a Latin root
that is still ongoing today. Concurrently, a
meaning “stretched apart”, which in botany
non-selective evolution process was proposed
refers to the usually wide angle at which
by Went (1971): the horizontal transfer of
branches of these species grow from the
“divaricate” genes; it however was strongly
stem on which they originate. Indeed, the
criticised on theoretical grounds (Tucker
branching angle of divaricating species is on
1974; Greenwood & Atkinson 1977) and
average more than 70°, sometimes over 90°
has not been empirically investigated so far.
(Bulmer 1958; Greenwood & Atkinson 1977),
Rationale for and content of this review whereas their broadleaved relatives branch
on average at < 55° (Kelly 1994). However,
Although about 120 years have passed since simplifying the definition of a divaricate
the first publications on the topic, the real species by its branching angle is misleading:
debate around the evolution of divaricates Pott & McLoughlin (2014) and Pott et al.
only started in the late 1970s. Yet, no recent (2015) discussed the evolutionary adaptations
literature review (e.g. Wilson & Lee 2012) of shrub or low-growing tree species of the
offers an exhaustive account of all the extinct gymnosperm family Williamsoniaceae
scientific material published about these by making a parallel between them and New
plants. The aim of this review is to provide Zealand divaricates, claiming that they share
a comprehensive resource for anyone with an similar architectures. Although the species
interest in divaricate plants. they described undeniably branched at wide
First, we review past attempts at defining angles, they did not look anything like what
the divaricate habit and describing its New Zealand researchers call “divaricates”:
variability in New Zealand. We propose they bore much larger leaves (4-25 cm long, cf.
a series of terms to try to standardise the < 2 cm in most New Zealand divaricates), and
vocabulary to be used when discussing these their branches were not interlaced. Likewise,
species (in bold in the text). We also report many examples of extant species can be cited
and discuss observations of divaricate-like as having wide branching angles while not
species overseas, compiling a list of such satisfying the definition of a divaricate, e.g.
occurrences. Araucaria heterophylla (Salisb.) Franco or Piper
We then review the published hypotheses excelsum (G.Forst.). Indeed, the divaricate
that have been formulated to explain how habit in New Zealand is also defined by a
such a diversity of architectures was selected collection of other traits, including: small
in the New Zealand flora, and comment on leaves (leptophyll and nanophyll classes of
the weight of evidence for or against each Raunkiær 1934); interlaced and abundant
hypothesis. Finally, we examine the handful branching; relatively long internodes
of studies that, rather than focusing on the compared to the size of their leaves (Kelly
evolution of these species, have looked at 1994 and references therein; Maurin & Lusk
developmental aspects of these peculiar 2020)—although some species show “short-
architectures. We conclude our review by shoot development” (Tomlinson 1978), i.e.
pointing out new areas of research that might stubby shoots with densely crowded nodes
enhance our understanding of divaricate and leaves. The exact set of features used
plants. to define the habit however varies between
authors (Kelly 1994; Grierson 2014; see TableMaurin & Lusk: Untangling the divaricate habit: review 3
1 in Supplementary Material for a list of traits thus do not prevent the outgrowth of lateral
used by past authors). Finally, New Zealand branches. This first definition of the term
divaricates are notably lacking in spines, “filiramulate” emphasised the wiry branches
except for Discaria toumatou Raoul which that may be flexuose to truly divaricating, and
has spinescent congeners in Australia and divaricate plants were therefore considered
South America. Some divaricating species, a type of filiramulate species. However, this
such as Melicytus alpinus (Kirk) Garn.-Jones definition of “filiramulate” has not been
and Aristotelia fruticosa Hook.f., have been widely adopted by the scientific community.
considered spinescent by some authors (e.g. The lack of a consensus word-based
Greenwood & Atkinson 1977; Burns 2016), definition of the divaricate habit led to two
but we argue that their pointed branchlets attempts to find a mathematical quantification
are not sharp enough to pierce the skin and of divaricateness. Atkinson (1992) focused on
therefore probably did not have the same branch density (number of lateral branches
adaptive value as actual wounding spines or subtended per cm of main branch) and
thorns. branching angle; Kelly (1994) also focused
Because the divaricate habit has evolved on branching angle, and included leaf size
independently multiple times in the New and density (the relative width of the leaves
Zealand flora, it appears under different to the size of the internodes that bear them).
structural forms that were tentatively grouped Although these two indices emphasise
by various authors to form classifications. different features of the divaricate habit,
Bell (2008) recognised four branching they correlate well for New Zealand species
pattern types in divaricate species: branching (Kelly 1994; Grierson 2014). In spite of these
at wide angles (e.g. Aristotelia fruticosa), zig- indices, which are rarely used in the literature,
zagging by sympodial (e.g. juvenile form of consensus definitions of the divaricate habit
Elaeocarpus hookerianus Raoul) or monopodial and its variations are still lacking.
(e.g. Muehlenbeckia astonii Petrie) growth, and
Heteroblastic divaricate species
“fastigiate”. The use of “fastigiate” (meaning
narrow branching angles) to categorise Although most of the species showing the
divaricate plants may seem paradoxical, divaricate habit keep it their whole life, some
but Bell’s (2008) example, Melicytus alpinus, heteroblastic species produce a divaricating
sometimes does show a fastigiate habit in form early in life, then later switch to a non-
shaded habitats. In our experience, however, divaricating form (Cockayne 1958). Very few
in sunny environments M. alpinus has wider quantitative data exist regarding the age before
branching angles and is compactly interlaced. the non-divaricating form appears (Table 1),
Tomlinson (1978) tried to assign divaricate which may depend on the degree of exposure
species to Hallé et al.’s (1978) architectural to sunlight in many cases (Cockayne 1958), or
models, without success. Halloy (1990) even on latitude at least in Sophora microphylla
defined five groups based on branching Aiton (Godley 1979). We propose referring to
patterns and assigned one species per group them as heteroblastic divaricate species; the
as examples, but his proposal has been largely term “habit-heteroblastic” used by Philipson
ignored. (1963) for such species is inadequate as it does
These variations around the features not mention “divaricate”, and the juvenile and
which characterise the divaricate habit led adults forms of some heteroblastic divaricate
Wardle & McGlone (1988) to propose species do not only differ in architecture but
the word “filiramulate” to describe lianes also in leaf shape (e.g. Pennantia corymbosa
and shrubs with reduced apical buds that J.R.Forst. & G.Forst.). Both forms often
have some (but not all) of the traits usually coexist on the same individual at least for
regarded as integral to the divaricate habit. some time, and the transition can be abrupt
These reduced buds exert a weakened apical (“metamorphic” species (Ray 1990), such
dominance (Wardle & McGlone 1988), and as in Pennantia corymbosa; see Figure 1 inNew Zealand Natural Sciences 46 (2021) 4
Table 1. Published quantitative measurements and estimations of the age reached by heteroblastic
divaricate species before their adult form appears.
Species Duration of the juvenile form Reference
Elaeocarpus hookerianus Raoul At least 60 years, depends on Cockayne (1958)
light conditions (source not
specified by the author)
Prumnopitys taxifolia (D.Don) (1) Up to 60 years (source not (1) Dawson & Lucas (2012)
de Laub. specified by the author) (2) Lusk (1989)
(2) At least 47 years (based on
ring counts)
Sophora microphylla Aiton (1) ca. 15 years (source not (1) Cockayne (1958)
specified by the author) (2) Godley (1979)
(2) variable according to location:
from absence of juvenile form in
some parts of the North Island,
to ca. 3.5 years in the Auckland
region and at least 23 years in the
south-east of the South Island
(based on field observations and
a common garden experiment)
Supplementary Material), or gradual with early form of some heteroblastic divaricate
transitional forms between the divaricating species are capable of flowering, such as
bottom and the non-divaricating top of the those of Pennantia corymbosa (Beddie 1958;
plant (“allomorphic” species (Ray 1990), Cockayne 1958) or Plagianthus regius (Poit.)
such as in Hoheria sexstylosa Colenso). Day Hochr. subsp. regius (Cockayne 1958): they
et al. (1997), studying the transition of the should therefore not be termed “juvenile”.
heteroblastic divaricate Elaeocarpus hookerianus However, alternative terms such as “young”
from its juvenile form to its adult form, and “old” carry ambiguities of their own,
described a distinctive transitional form so it is not obvious to us how to improve
characterised by a less plastic growth pattern upon “juvenile” and “adult”, which have
than the juvenile form, while not showing become deeply anchored in the literature. We
the morphological attributes that identify however recommend the use of juvenile/
the adult form. adult form instead of the more commonly
The ubiquitous use in the literature used juvenile/adult “stage” or “phase” to
of the adjectives “juvenile” and “adult” avoid the confusion between growth habit
(sometimes “mature”) to name, respectively, and reproductive state that Jones (1999)
the early divaricating form and the ultimate pointed out.
non-divaricating form of heteroblastic Two hypotheses have been proposed to
divaricate species, is potentially misleading. try to explain the origin of heteroblastic
Jones (1999) criticised the use of “juvenile” divaricate species:
to describe early forms of heteroblastic
species because it better characterises a phase 1. Hybridisation between a divaricate
of plant development that is incapable of species and a non-divaricate relative
sexual reproduction. She therefore suggested
that “juvenile” should be restricted to non- It is well known that some divaricate species
flowering stages of heteroblastic species. hybridise with broadleaved congeners (e.g.
Yet, it was observed in New Zealand that the Dansereau 1964; see lists of known (andMaurin & Lusk: Untangling the divaricate habit: review 5
potential) hybrids compiled by Cockayne arose from heteroblastic divaricate ancestors
1923, Cockayne & Allan 1934 and Greenwood which later lost their forest-adapted adult
& Atkinson 1977). These hybridisation events form in response to new selective pressures
were hence proposed as a source for the in more open environments. It was first
origin of heteroblastic divaricate species suggested by Cockayne (1911, p. 25–26;
(Godley 1979; 1985). Carrodus (2009) 1958, p. 141) and further developed by Day
addressed the question of whether Pittosporum (1998a). It is difficult to see how to test such a
turneri Petrie, a heteroblastic divaricate hypothesis, which may explain why it has not
small tree, is a hybrid between Pittosporum been the subject of published research so far.
divaricatum Cockayne, a divaricating shrub,
The divaricate habit in New Zealand and overseas
and Pittosporum colensoi Hook.f., a broadleaved
tree. The study used plastid and nuclear DNA Variations of the divaricate habit are found
markers as well as a morphological analysis in ca. 81 taxa in New Zealand (Appendix
and found evidence supportive of such 1), including heteroblastic divaricate taxa.
an event, e.g. that P. tuneri shows an ISSR 80 are Eudicots, one is a Gymnosperm, and
band and morphological traits (for example they represent 20 families. According to
in leaves, flowers and fruits) that combine statistics about the New Zealand vascular
those of the putative parents. They however flora produced by De Lange et al. (2006),
suggested more investigation: their cross- this number represents almost 13% of
pollination experiments between P. divaricatum indigenous woody spermatophytes. We
and P. colensoi did not produce progeny, and refer to all these species as divaricates, a
given the limitations of the ISSR technique term that encompasses architectures that
they recommend using more nuclear markers fall on a spectrum with two extremes. On
in more individuals. Shepherd et al. (2017) and one end, there are the true divaricates (or
Heenan et al. (2018) used chloroplast DNA truly divaricating species), i.e. species with
and microsatellite markers respectively to the most characteristic traits of the habit
study hybridisation and introgression events (such as tightly interlaced tough branches
in New Zealand Sophora L.: even though their with relatively long internodes compared
findings showed that these species hybridise to leaf size, and leaves < 2 cm in length);
readily, they reported little support for the typically shrubs that are common in open
hypothesis that the heteroblastic divaricate environments such as forest margins. To
species Sophora microphylla arose through characterise the other end of the spectrum,
hybridisation between divaricate species we propose to use the term semi-divaricate
Sophora prostrata Buchanan and the non- as used by Greenwood & Atkinson (1977);
divaricate species Sophora tetraptera J.F.Mill. these are species with traits that are not as
However, as Godley (1985) makes explicit, typical as the traits of the true divaricates,
his hypothesis allows for multiple generations such as slender branches in a more open
after an initial hybridisation and for selection architecture, and larger leaves—sometimes
of the heteroblastic divaricate form from species that appear clearly divaricate in open
a variable population of hybrid derivatives areas tend towards a semi-divaricate habit
(such as a hybrid swarm). Therefore, genetic when growing in the shade (Philipson 1963;
signal of a hybrid origin might be weak Christian et al. 2006; pers. obs.).. Furthermore,
and difficult to detect in studies employing we use the term divaricate habit to refer to
only modest numbers of genetic markers. the habit as a phenomenon, which manifests
itself through a variety of architectures that
2. Neotenous loss of a putative adult we refer to as divaricating habits.
non-divaricate form Although divaricates are present in a wide
range of environments throughout New
A mirror image of the previous hypothesis, Zealand, several environmental patterns
this hypothesis states that divaricate species in their abundance have been noted. TheyNew Zealand Natural Sciences 46 (2021) 6
can be found in most forest types and reported by Tucker (1974), and the South
successional shrublands (Wardle 1991), African shrub species with dense, cage-like
from the coast to alpine environments architectures studied by Charles-Dominique
(Greenwood & Atkinson 1977). Divaricates et al. (2017). Most overseas divaricate-like
have been reported as especially common in plants also differ notably from all but one
open environments such as forest margins New Zealand divaricates by the presence of
(McGlone & Webb 1981), though relevant wounding spines. A striking example is the
quantitative data are lacking. The percentage African boxthorn (Lycium ferocissimum Miers;
of divaricate species in woody assemblages see Figure 2 in Supplementary Material), a
increases from north to south (McGlone South African species naturalised in New
et al. 2010). Quantitative analyses have Zealand, which has tough interlaced branches
shown strong associations with frosty (and similar to those of some New Zealand
to some extent, droughty) climates such as divaricates but bears sharp spines. However,
are typical of the eastern South Island (Lusk this spinescence can sometimes be rather
et al. 2016; Garrity & Lusk 2017) where weak, for example in Australian species of
notably divaricate species often comprise the Melicytus J.R.Forst. & G.Forst. (Stajsic et al.
majority of arborescent assemblages (Lusk et 2015). There are however some overseas
al. 2016). It has been stated that divaricates divaricate look-alikes that show the same
are commonest on fertile young soils, such traits as New Zealand divaricates, for example
as those derived from recent alluviums or Tetracoccus hallii Brandegee (Picrodendraceae),
volcanic ashes (Greenwood & Atkinson 1977; a non-spiny shrub with seemingly tough,
McGlone et al. 2004). Consistent with this interlaced branches, branching at wide angles
proposal, the largest known concentrations and bearing small leaves (descriptions and
of divaricate species occur on alluvial terraces pictures from SEINet Portal Network 2020
derived from mudstone in the Rangitikei and and Calflora 2020) from south-west USA
Gisborne areas (Clarkson & Clarkson 1994). (distribution data from GBIF 2020 and
However, an analysis of > 1,000 plots by Calscape 2020).
Lusk et al. (2016) did not detect a significant We propose a list of the species that the
association with terraces, or with any other studies cited above claim as “divaricate” and
topographic position. that we agree do resemble the architectural
Even though broadly similar plants occur models we see in New Zealand divaricates
in many other regions of the world, few of (Appendix 2). We sug gest the name
them show the full range of traits that are divaricate-like to describe these species in
typical of New Zealand divaricates. Species order to emphasise their resemblance with
showing aspects of the divaricate habit have New Zealand divaricates, yet stressing the fact
been reported from Madagascar (Grubb that they often present distinguishing features
2003; Bond & Silander 2007), Patagonia (discussed above) and that they evolved
(Wardle & McGlone 1988; McQueen 2000) in environmental conditions that were
or South America in general (Böcher 1977), somewhat different from those experienced
mainland Australia and Tasmania (Bulmer by the ancestors of New Zealand divaricates
1958; Mitchell et al. 2009; Thompson 2010; (reviewed below).
Stajsic et al. 2015), Arizona and California in
the USA (Carlquist 1974; Tucker 1974) and
New Guinea (Lloyd 1985). The reported
species and their close relatives indeed
show branching patterns similar to what
is seen in New Zealand divaricates, but
they often present rather large leaves. This
is for example the case with the North
American Quercus dunnii Kellogg ex Curran,Maurin & Lusk: Untangling the divaricate habit: review 7
A review of theories about evidence show that New Zealand was not
the evolution of New Zealand completely submerged during the Late
divaricates Oligocene (reviewed by Mildenhall et al.
2014), particularly the 23 Myo Foulden
Maar deposit (near Middlemarch, Otago),
The climatic hypothesis which notably contains fossils of diverse
land plants (e.g. Lee et al. 2016). Moreover,
Since its Upper Cretaceous separation from
recent molecular dating of the age of New
Gondwana (Wallis & Trewick 2009), New
Zealand lineages strongly suggest that some
Zealand has undergone wide-ranging climatic
extant terrestrial plant and animal groups
changes. There is some debate as to the
most probably originated from a Gondwanan
climate of the Upper Cretaceous: some argue
vicariance (Wallis & Jorge 2018; Heenan &
this period was probably warmer than today
McGlone 2019).
(e.g. Fleming 1975), others that it was similar
Diels (1896) was the first to hypothesise
to present-day climates (e.g. Mildenhall 1980;
an important role of Pleistocene climate
Kennedy 2003). Hornibrook’s (1992) review
in shaping the modern New Zealand flora,
of marine fossil evidence indicates mostly
and as far as we are aware his work is the
subtropical climates during the Paleogene,
first attempt to explain the evolution of
although a sudden cooling event may have
the divaricate habit. He proposed that, by
occurred around the Eocene-Oligocene
reducing transpiration, the divaricate habit
boundary; temperatures then warmed to
helped plants cope with droughty climates
a local peak around 16 Mya, during the
created in the eastern South Island by the
Miocene; the climate remained subtropical
uplift of the Southern Alps. Cockayne
until a Late Miocene cooling, with further
(1911) proposed that the divaricate habit
cooling from the Pliocene. The combined
was a response to past windy and droughty
effects of this global cooling and of the
Pleistocene steppe climates, especially in the
rapid uplift of the Southern Alps during the
South Island. Similarly, Rattenbury (1962)
Kaikoura Orogeny (Batt et al. 2000) created
hypothesised that the divaricate habit was
local frosty and droughty environments,
an adaptation to dry or cool Pleistocene
especially in the eastern South Island. These
climates, and suggested an effect of the cage-
new climates are likely to have reduced plant
like architecture as a windbreak, reducing
growth on many sites (Lusk et al. 2016), as
transpiration. Wardle (1963) suggested that
shown by comparisons of juvenile annual
the divaricate habit continues to be adaptive
height growth rates of the small broadleaved
in the present-day drier forest and shrub
tree Aristotelia serrata J.R.Forst. & G.Forst. on
environments of eastern New Zealand.
modern sites that differ in growing season
McGlone & Webb (1981) fur ther
length (Bussell 1968; Anton et al. 2015).
developed the climatic hypothesis, joining
Besides these climatic variations, a
the debate started by Greenwood and
progressive submergence greatly reduced
Atkinson with the moa-browsing hypothesis
the extent of the New Zealand landmass
(Greenwood & Atkinson 1977; see next
from the Upper Cretaceous to the Early
section). They suggested that the divaricate
Miocene (85–22 Mya; Landis et al. 2008). It
habit represents the response of the “largely
reaching a peak around 25–23 Mya known as
subtropical” Tertiary flora of the isolated
the Oligocene marine transgression (Cooper
New Zealand archipelago to the near-treeless
1989), at which point the surface of the New
glacial periods of the Pleistocene; this habit
Zealand mainland was about 18% of its
may have protected growing points and leaves
present-day surface area (Cooper & Cooper
from wind abrasion, desiccation and frost
1995). Landis et al. (2008) argued that, at that
damage, which occurred unpredictably in
time, New Zealand was probably completely
the weakly seasonal New Zealand climates
submerged, but this idea is now clearly
of the Quaternary. McGlone & Webb (1981)
refuted. Geological and paleobiologicalNew Zealand Natural Sciences 46 (2021) 8
also argued that the cage-like architecture The photoprotection variant of the climatic hypothesis
of the divaricate habit also provides a
Howell et al. (2002, see also Howell 1999),
milder microclimate within the plant which
proposed that the shading of inner leaves by
promotes higher rates of photosynthesis. The
the cage-like divaricate architecture protects
transition from the juvenile form to the adult
them from high irradiance on cold mornings
form in heteroblastic divaricate species occurs
after frosts, thus minimising photoinhibition
above the height of the most damaging frosts
and photodamage. It is a derivative of the
during temperature inversions on clear nights,
climatic hypothesis that includes the effect of
and the absence of the habit on offshore and
solar radiation as a selective pressure under
outlying islands can be explained by their
stressfully cold climatic conditions. Howell
more oceanic, hence milder and less frosty,
et al. (2002) tested this hypothesis with an
climates. Burns & Dawson (2009) however
experiment involving the pruning of the
noted that the heteroblastic divaricate species
outer branches of three divaricate species,
Plagianthus regius from the mainland has a
which resulted in a reduced photosynthetic
heteroblastic divaricate subspecies (P. regius
capacity of the inner leaves of these shrubs
subsp. chathamicus (Cockayne) de Lange) on
for at least 3 months. This experiment was
the historically avian-browser-free Chatham
criticised by Lusk (2002), who pointed out
Islands: they propose that, because P. regius is
that the failure to include non-divaricate
a recent immigrant on the Chatham Islands,
species as a control undermined the authors’
its juvenile form has not been counter-
conclusions: without further research, we
selected yet.
cannot know if non-divaricate plants would
The climatic factors suggested as selective
respond in a similar way to pruning of their
forces are certainly not peculiar to New
outer branches.
Zealand, whereas divaricate-like forms are
much less common in other regions with Empirical appraisal of the climatic hypothesis
similar climates (Dawson 1963). McGlone
& Webb (1981) argued that what made Experimental tests have produced little
New Zealand unique in the evolution of its support for the climatic hypothesis. Although
subtropical flora in response to the cold, dry past climatic conditions cannot be reliably
and windswept environments that appeared reproduced in a controlled experiment, it is
during the Quaternary was its isolation from possible to estimate the differential response
sources of steppe-adapted floras, apparently of divaricate and non-divaricate species when
believing that such floras might have provided they are subjected to present-day climatic
plants with more conventional physio- conditions similar to those hypothesised to
morphological responses to cold, dry climates. have selected the divaricate habit during the
This argument appears to overlook the fact Pleistocene.
that divaricate shrubs are also common in the Kelly & Ogle (1990) were the first to
Patagonian steppe, although those species publish a test of the response of divaricating
are invariably spinescent (McQueen 2000). habits to climatic conditions. They studied
Furthermore, if wind was one of the drivers the effect of air temperature, humidity, frost
of the evolution of the divaricate habit, it is and wind on internal and external leaves of
strange that few divaricate species are found a divaricate species and both juvenile and
in some very windy parts of New Zealand adult forms of a heteroblastic divaricate
(Greenwood & Atkinson 1977): although species. While they did not show a significant
they are often prominent in the vegetation of difference in leaf temperature and air
windswept areas such as Cook Strait (Wardle humidity between the inside and the outside
1985), they present a low species richness of divaricating habits, they did show that the
there (Gillham 1960). habit provides some protection against frost.
Keey & Lind (1997) used four species
showing various divaricating habits to test the
effect of different branching architectures onMaurin & Lusk: Untangling the divaricate habit: review 9
the surrounding airflow patterns. Although especially stressfully cold temperatures. In
they did not compare these species to non- parallel, Schneiderheinze (2006) studied
divaricate species, they showed that dense photoinhibition in divaricate and non-
branching patterns produce calmer zones, divaricate species under high light loads and
which may imply that they create a more other stressful conditions, such as drought.
favourable growing environment for leaves She found plants of both habits showed
and other fragile organs by reducing wind similar levels of photoinhibition under high
damages. irradiance, whether the plants were water-
Darrow and colleagues experimentally stressed or not. Here again, the hypothesis
compared the frost resistance (2001) and as formulated by Howell et al. (2002; i.e.
water use efficiency (2002) of juvenile and protection from photoinhibition under cold
adult forms of heteroblastic species, most conditions) was not tested, but the study still
of them divaricate at a juvenile stage. Darrow provided a valuable insight into the absence
et al. (2002) found that most (though not all) of significant photoprotection in divaricate
divaricate juvenile forms had lower water species compared to their non-divaricate
use efficiency than the corresponding adult relatives.
forms, concluding their results were not Recently, an observational approach was
consistent with the climatic interpretation taken by Lusk et al. (2016), who examined the
of the divaricate form. Darrow et al. (2001) environmental correlates of the proportion of
compared the frost tolerance of the leaf divaricate species in arborescent assemblages
tissues of juvenile and adult forms of five throughout the main islands of New Zealand.
heteroblastic divaricate species by chilling They concluded that divaricate species are
leafy twigs overnight in thermostatically generally more diverse and prominent at
controlled freezers. However, their findings frosty and droughty sites. Garrity & Lusk
are of limited relevance to the climate (2017) also used an observational approach by
hypothesis, as this approach does not address correlating climatic data with the distribution
the effect of leaf size on night-time chilling of 12 congeneric pairs of divaricate and
under a clear sky (cf. Lusk et al. 2018), larger-leaved species of the main islands of
nor any potential effect of stem vascular New Zealand. They found that divaricate
anatomy on freeze-thaw embolism. In a species were significantly favoured by colder
similar vein, Bannister et al. (1995) studied the mean annual temperatures, and especially by
development of frost tolerance of detached colder minimum July temperature, but there
leaves of some divaricate and non-divaricate was little evidence of an association with
species of Pittosporum Banks & Sol. ex Gaertn. droughtier environments. Their results also
over the course of autumn and winter. As was showed little support for the photoprotection
the case for Darrow et al. (2001) this study hypothesis, as divaricate species tended
of tissue-level responses to frost did not test to predominate in cold environments
the potential roles of any of the characteristic irrespective of winter solar radiation levels.
leaf or stem traits of divaricates in conferring These two different observational approaches
frost resistance . concur in showing that short frost-free
A test of the photoprotection hypothesis periods and cold climates in general favour
was provided by Christian et al. (2006), who the abundance and diversity of divaricate
compared carbon gain versus structural species, but do not quite agree on the effect
costs of three congeneric pairs of divaricate of drought. Given the limited number
and non-divaricate species under different of species encompassed by Garrity &
intensities of light exposure. They showed Lusk (2017), as well as evidence that the
that the costs of divaricating habits may largest concentrations of divaricate species
be too high to be compensated by the occur on middle North Island sites subject
photoprotection it provides, although to significant water deficits (Clarkson &
they did not subject their samples to Clarkson 1994), the balance of the evidenceNew Zealand Natural Sciences 46 (2021) 10
indicates that both frost and drought favour about how the ancestors of moa reached
divaricate species. New Zealand (Allentoft & Rawlence 2012):
Finally, a key component of the divaricate they may have inhabited the New Zealand
habit is small leaf size, which is known to landmass from the time it started to separate
be advantageous under harsh climates. A from Gondwana about 80 Mya (the “Moa’s
study by Lusk et al. (2018) compared leaf Ark” of Brewster 1987); alternatively their
temperature during clear winter nights in ancestors might have reached New Zealand
relation to leaf size for 15 native New Zealand either by walking before 60 Mya, when the
species, including four congeneric pairs of New Zealand landmass was still connected to
divaricate and non-divaricate species. They a disintegrating Gondwana, or by flying after
observed that small leaves chilled significantly the complete separation. This last possibility
less than large leaves. Their conclusions is consistent with recent molecular evidence
provide experimental support to leaf energy that the closest living relatives of moa appear
balance theory, which predicts that large to be tinamous (Phillips et al. 2010; Mitchell
leaves should be more vulnerable to frost et al. 2014), a group of volant birds. If the
because they cool below air temperatures on earliest ancestors of moa to inhabit Zealandia
frosty nights whereas the smallest leaves stay were volant, fossil evidence suggest that their
close to air temperature (Parkhurst & Loucks descendants have been large flightless birds
1972; Wright et al. 2017). Although this since at least 16-19 My ago (Tennyson et al.
effect does not explain the three-dimensional 2010). All moa species were extinct by about
structure of the divaricate habit, it suggests the mid-15th century CE (Perry et al. 2014),
that the characteristically small leaves of apparently because of hunting (Allentoft et
divaricates may have provided an adaptive al. 2014).
value in open habitats with short annual Moa subfossil remains are more common
frost-free periods (see also Lusk & Clearwater on the South Island than on the North
2015, a similar but less conclusive study on Island (Anderson 1989); moreover, they are
a smaller scale). Additionally, a study of the more concentrated in the east of the South
relationship between leaf dimensions and Island (Anderson 1989). However, this does
environmental variables in South African not necessarily mean that moa were more
species of Proteaceae concluded that small abundant in the eastern South Island than
leaves promotes convective heat dissipation elsewhere in the country, since the subfossil
under dry conditions and limited wind, record is probably influenced by preservation
enabling them to avoid overheating when biases: natural moa bone deposits are mainly
water shortage forces stomatal closure in alkaline swamps and limestone caves, which
(Yates et al. 2010). This effect was confirmed are near-ideal preservation environments
on Australian Proteaceae by Leigh et al. (Atkinson & Greenwood 1989) that happen
(2017). The small size of the leaves of most to be more common in the eastern South
divaricates may therefore enable them to Island than in most other parts of the country
cope with drought better than large-leaved (Anderson 1989). Furthermore, an estimation
competitors. of population size and distribution of the
different moa species based on mitochondrial
The moa-browsing hypothesis
DNA and fossil record of Dinornis spp.
“Moa” is the Māori name for a group of suggests, in contrast, that moa populations
now-extinct large (1-3 m and 10-250 kg; were more numerous on the North Island
Atkinson & Greenwood 1989; Worthy & than on the South Island (Gemmell et al.
Holdaway 2002) flightless birds (“ratites”) of 2004). Therefore, it seems difficult at present
the endemic order Dinornithiformes. Nine to draw clear conclusions about geographic
species are currently recognised, belonging variation in moa densities.
to six genera and three families (Worthy & Although the potential influence of moa
Scofield 2012). There are several hypotheses browsing on the evolution of the divaricateMaurin & Lusk: Untangling the divaricate habit: review 11
habit had been suggested by previous authors (McGlone & Clarkson 1993), the largest
(e.g. Denny 1964; Carlquist 1974; Taylor known concentrations have been reported
1975), Greenwood & Atkinson (1977) were from fertile terraces derived from mudstone
the first to fully develop and argue this idea. (Clarkson & Clarkson 1994). On the other
First postulating that moa fed by clamping hand, Greenwood & Atkinson (1977) noted
and pulling vegetation in the same manner that divaricates are largely absent from areas
as present-day ratites, they hypothesised where moa did not live, such as offshore
that the tough and highly tensile branches islands, or where moa could not reach them,
of many divaricate species are difficult to such as growing on cliffs or as epiphytes.
tear off, while the interlaced structure kept Although Myrsine divaricata A.Cunn. is
leaves and growing tips out of easy reach. abundant on some of the subantarctic islands
Hence, browsing on these plants would be of New Zealand (McGlone & Clarkson 1993;
less energetically rewarding than browsing on Meurk et al. 1994), which are unlikely to have
broadleaved species. Greenwood & Atkinson harboured moa, Greenwood & Atkinson
(1977) did not completely exclude a cutting (1977) attributed such occurrences to recent
ability of moa beaks, later acknowledging that colonisation from the mainland. Kavanagh
the feeding behaviour of moa could not be (2015) lent support to this interpretation by
confidently inferred because fossil skulls do comparing some traits used to describe the
not retain all the relevant tissues (Atkinson & divaricate habit between related species of
Greenwood 1989). A recent study simulating New Zealand mainland and Chatham Island
the force of moa jaw muscles however (historically moa-free, with a flora largely
concluded that different moa species fed derived from the mainland): he concluded
in various different ways, including cutting that the absence of moa may have relaxed
(Attard et al. 2016). This appears to confirm the selection for traits that deterred moa
the findings of studies of moa gizzard browsing on the main islands of New
contents, which concluded that that divaricate Zealand.
twigs consumed by moa had been sheared Greenwood & Atkinson (1977) also
rather than broken off (Burrows 1980; 1989; examined the bearing of the height of
Burrows et al. 1981). These findings were later transition between the juvenile in adult forms
corroborated by a study of coprolites (Wood in heteroblastic divaricate species on their
et al. 2008), yielding the same conclusion that hypothesis. They claimed that, in such species,
divaricate species were by no means exempt the shift from the juvenile divaricate form
from moa browsing (reviewed by Wood et to the adult non-divaricate form happens
al. 2020). around 3-4 m high; this height corresponds
Moreover, Greenwood & Atkinson (1977) to the approximate height of the tallest moa,
used evidence from the distribution of implying that the adult form in these species
divaricate plants to support their hypothesis. only appears at heights where it is safe from
One the one hand, they pointed out that browsing. Burns & Dawson (2006) brought
divaricate plants often grow on lowland support to this claim from New Caledonia:
river terraces and swamps, which offer they mentioned that heteroblastic species
high nutrient levels and hence high plant there (which do not have a divaricating
productivity and nutrient content. They juvenile form) seem to shift form at about
explained that divaricate species should be the estimated height of the flightless birds
more subjected to moa browsing in such which once lived there, although they called
places, a sensible claim given that at least some for quantitative support for this observation.
studies show a positive correlation between There are however multiple counter-examples
herbivore abundance and soil fertility (e.g. to Greenwood & Atkinson’s (1977) claim.
Kanowski et al. 2001). Even if divaricate Field observations sometimes reveal that
species have been reported from low fertility the shift can happen significantly lower; for
soils, such as the acidic soils of Stewart Island example, Cockayne (1911) reported thatNew Zealand Natural Sciences 46 (2021) 12
the shift in Sophora microphylla can happen Lowry’s view (Atkinson & Greenwood 1980).
as low as 1.4 m, and we observed a shift in Consequently, this view raised the question
Pennantia corymbosa happening at about 2 m of why the divaricate habit, if it is not a
high (Figure 1 in Supplementary Material). specialised moa-deterring adaptation, is much
Conversely, some homoblastic divaricate scarcer in other regions where non-ratite
species can reach heights significantly above browsers existed (McGlone & Webb 1981).
the size of the tallest moa without showing Indirect support for the moa-browsing
any relaxation of their divaricating habit; hypothesis came from a fossil of a small-
McGlone & Clarkson (1993) report such leaved woody species with wide-angle
instances with individuals of Coprosma opposite branching that was discovered by
crassifolia Colenso, Melicope simplex A.Cunn. Campbell et al. (2000). It was estimated to
and Myrsine divaricata more than 5 m high; date from 20-16 Mya, which corresponds
individuals of the latter species exceeding to the Early Miocene, whereas the climatic
this height were also recorded by Veblen & conditions usually put forward as the drivers
Stewart (1980). of the evolution of the divaricate habit did
Finally, a crucial point of Greenwood & not occur before the Pliocene (i.e. not before
Atkinson’s (1977) argument is the fact that 5.333 Mya, Cohen et al. 2013, updated).
the New Zealand flora is unique in having Despite the absence of information about
co-evolved with ratites but without browsing the three-dimensional structure of the
mammals. This phenomenon did not occur plant when alive, 12 out of 15 experts they
in areas where divaricate-like species co- consulted agreed it was most likely a divaricate
evolved with ratites: in Madagascar, now- species (potentially extinct), and had rather
extinct elephant birds shared the island with varied ideas about what genus it could belong
giant tortoises and giant lemurs (Bond & to. They noted the presence of “small acute
Silander 2007); in Patagonia, Darwin’s rhea broken processes protrud[ing] from the
grazed side-by-side with diverse mammals, branchlets at irregular intervals”, which look
such as equiids, camelids and giant ground like spines even though they are not opposite.
sloths (McQueen 2000); in Australia, emus Even though the processes might have been
coexisted with many different herbivorous defensive spines that would be of little use
mammals, mostly marsupials (Roberts et against moa beaks, this discovery appears
al. 2001). Although these regions have all consistent with the moa-browsing hypothesis.
undergone megafaunal extinctions, they According to the moa-browsing hypothesis,
still host browsing mammals, and with the the divaricate habit could be nowadays seen
exception of Madagascar they have retained as an anachronism (Greenwood & Atkinson
their ratites as well. No ratites or ratite fossils 1977). As such, it was hypothesised that
are known from North America; they are divaricate species may not be adapted to the
known only from former Gondwanan lands current browsing pressure of introduced
(Briggs 2003). mammals because their costly ratite-resistant
Greenwood & Atkinson (1977) originally architecture was thought to be useless against
hypothesised that the divaricate habit evolved mammals (Bond et al. 2004). Diamond
as a deterrent to moa browsing. Lowry (1980) (1990) imported the concept of “ghost”
instead suggested that the main effect of the from overseas cases of anachronisms (later
divaricate habit is to help the plant survive reviewed by Barlow 2000) when defending
browsing by spacing and multiplying palatable the hypothesis that divaricates are adapted
growing tips, with a side-effect of making the to a now-extinct fauna. However, the
browsing less energetically rewarding. This conclusions of Pollock et al. (2007) about the
idea that the divaricate habit enables plants preferences of ungulates for New Zealand
to survive rather than to prevent browsing woody plants, as well as a study by Lusk
led Atkinson and Greenwood to reconsider (2014) on the regeneration of divaricate and
their 1977 hypothesis by acknowledging non-divaricate species in a forest remnantMaurin & Lusk: Untangling the divaricate habit: review 13
that had been subject to ungulate browsing New Zealand landmass as early as 80-60 Mya
for decades, indicate that the divaricate habit (reviewed by Allentoft & Rawlence 2012),
may also be effective in deterring mammal the divaricate habit may not have become
browsing. Ungulates indeed tend to avoid advantageous as an anti-browsing defence
some (though not all) divaricate species until until Plio-Pleistocene climatic constraints
more attractive foods are depleted (Forsyth on plant growth resulted in juvenile trees
et al. 2002; Lusk 2014). being exposed for longer to ground-dwelling
browsers. During this period the combination
Experimental appraisal of the moa-browsing
of global cooling (Hornibrook 1992) and
hypothesis
rapid uplift of the Southern Alps (Batt et al.
The moa-browsing hypothesis was first tested 2000) created widespread frosty, droughty
experimentally by Bond et al. (2004), who environments in the eastern South Island.
fed juvenile and adult form foliage of two The relatively fertile alluvial soils of these
heteroblastic divaricate species to present- environments may have attracted high levels
day ratites (emus and ostriches). They found of browsing, but frost and drought would
that the high tensile strength of divaricate have reduced the ability of juvenile trees
branches reduces breakage, that the high to grow rapidly out of the browsing zone,
branching angles make the twigs difficult even in well-lit microenvironments such as
to swallow because birds cannot use their treefall gaps. Evidence for a much earlier
tongue to properly orient the twigs, and that origin of divaricate plants, for example in
small and widely spaced leaves increase the the more benign climates of the Miocene or
time and the energy required to consume leaf Oligocene, would refute both this hypothesis
biomass. These results brought support to the and the original climate hypothesis, and would
hypothesis that the divaricate habit represents point to moa browsing as the sole driver of
an adaptation to deter moa browsing. divaricate evolution if no other factor can
However, whether the feeding behaviour be identified.
of the present-day ratites reliably reflect the
The light trap hypothesis and its appraisal
feeding behaviour of extinct moa is a matter
of debate (reviewed above). The light trap hypothesis, formulated by Kelly
A more elaborate cafeteria experiment was (1994), relies on the conclusions of Horn
conducted a few years later by Pollock et al. (1971) that a multi-layered leaf distribution
(2007), comparing the offtake of deer, goats (i.e. leaves distantly scattered among multiple
and ostriches from five divaricate species layers in the canopy) is more efficient at
compared to five congeneric non-divaricate capturing a higher proportion of sunlight
species. Their general finding is that features than mono-layered architectures (i.e. leaves
of the divaricate habit, such as small leaves distributed in a dense layer, the umbra of
and stem toughness, deter ungulates as well the outermost leaves completely obscuring
as ratites. the innermost leaves). Photosynthesis of
most plants is indeed saturated well below
The moa-climate synthetic hypothesis
full sunlight, the saturation point varying
The idea that selection for the divaricate habit with, for example, species’ successional status
may have been driven by both past climatic (e.g. Bazzaz & Pickett 1980). The scattered
conditions and the effect of moa browsing distribution of the leaves of divaricates
has been suggested several times since the over multiple branch layers therefore allows
debate started (Wardle 1985; 1991; Cooper inner leaves to be in the penumbra of the
et al. 1993; Bond & Silander 2007). Lusk et outer leaves, thus better distributing light
al. (2016) proposed a synthetic hypothesis harvest throughout the canopy. The light
with a specific mechanism integrating trap hypothesis appears consistent with a
browsing and climatic factors. Although modelling study of the impact of penumbral
the ancestors of moa may have reached the effects on shoot-level net carbon gain ofNew Zealand Natural Sciences 46 (2021) 14
conifers (Stenberg 1995) which, like New Moreover, he suggested that this sequential
Zealand divaricates, have small effective branching is characterised by a lack of
leaf diameters that result in short shadows; organisational control that translates into
this modelling however does not explain a dimorphism between orthotropic and
the potential advantage of the architectural plagiotropic branches. He recommended
structure of divaricating habits. Moreover, the study of the changes in the branching
even though penumbral effects are likely to sequence of many divaricate species over
result in higher carbon gain per unit area of their lifetime, as he believed this could be
foliage in small-leaved species growing in the only way to understand how the diversity
high light, Christian et al.’s (2006) data suggest of divaricating habits was produced under a
that this advantage will be outweighed by the possibly single selective pressure, and to draw
much higher (ca. threefold) leaf area ratio of general conclusions about their development.
congeneric broadleaved species, resulting in Subsequently, the development patterns
higher net carbon gain per unit of biomass of a few divaricates were studied in the
in the latter. In divaricate species, this effect 1990s. The species were: Muehlenbeckia astonii
might be at least partially compensated by (Lovell et al. 1991); the juvenile form of
photosynthesis in stems, brought to light in Elaeocarpus hookerianus (Day & Gould 1997;
one instance so far: the juvenile form of the Day et al. 1998; Day 1998a), Carpodetus
heteroblastic divaricate Prumnopitys taxifolia serratus J.R.Forst. & G.Forst. (Day 1998a; b)
(Banks & Sol. ex D. Don) de Laub. (Mitchell and Pennantia corymbosa (Day 1998c); Sophora
et al. 2019). More divaricate species will prostrata and the juvenile form of Sophora
need to be investigated to determine how microphylla (Carswell & Gould 1998). Overall,
widespread stem photosynthesis is among these studies concluded that such a growth
divaricates. However, why would divaricating pattern, with many growing points scattered
habits be scarce or absent in most other across the plant’s crown, offers a plastic
regions of the world if sunlight were the structure that can more easily accommodate
main driver of the evolution of these peculiar changes in environmental conditions (e.g.
architectures in New Zealand, where solar forest canopy gap versus closed canopy
irradiance levels are similar to those of other or seasonal changes in environmental
regions at comparable latitudes (Solargis conditions). These case studies also agreed
2020)? The light trap hypothesis does not that the lack of apical dominance plays a key
appear to offer a satisfying explanation of role in the establishment of the divaricating
the evolution of the New Zealand divaricates. habits they observed.
In parallel to the study of developmental
Insights into the development of divaricate branching
patterns, a handful of studies looked into
patterns
the hormonal control of the divaricate
If the debate surrounding divaricate plants habit. Horrell et al. (1990) showed that a
has mainly focused on how the divaricate gibberellic acid treatment on cuttings of
habit has evolved, a handful of studies looked the adult form of Pennantia corymbosa and
into describing the range of growth patterns Carpodetus serratus tends to revert them to
that give rise to the spectrum of divaricating their juvenile form. This phenomenon did
habits, and how such patterns translate into not occur in Elaeocarpus hookerianus, a result
adaptations to local environments. later confirmed by Day et al. (1998) with
Tomlinson (1978) examined bifurcation treatments of adult cuttings with gibberellic
ratios of 18 New Zealand divaricates, acid and other growth factors, including
including two heteroblastic divaricate a cytokinin. Day et al. (1998) also showed
species. He concluded that the interlaced that the adult form is not precociously
structure of most divaricates is a consequence triggered in E. hookerianus seedlings by these
of a sequential branching which may be treatments. In Sophora, a treatment with
supplemented by reiterative branching. 6-benzylaminopurine (a cytokinin) reinforcesMaurin & Lusk: Untangling the divaricate habit: review 15
the divaricateness of the juvenile form of nevertheless do not resolve the blurry
Sophora microphylla (Carswell et al. 1996). boundary between true divaricates and semi-
Qualitative and quantitative measurements in divaricates, like any categorisation involving
E. hookerianus showed that the leaves of the a degree of subjectivity.
divaricating juvenile form contain more active In spite of rather extensive experimental
cytokinins than the non-divaricating adult and observational evidence, no hypothesis
form or transitional form leaves (Day et al. about the evolution of divaricates in New
1995, reviewed by Jameson & Clemens 2015). Zealand has been decisively favoured over
A similar yet more questionable conclusion another. Among the most plausible hypotheses
was drawn from a comparison of the ratio however, the moa-browsing hypothesis seems
of active to storage forms of cytokinin more supported than the climatic hypothesis,
between divaricate and non-divaricate forms although neither are fully satisfying on their
in Sophora species (Carswell et al. 1996). In own. The synthetic moa-climate hypothesis
contrast with the heteroblastic divaricate has not been much discussed or tested so
species studied, the levels of cytokinins are far, but given the evidence of both the
relatively low in the divaricate species Sophora moa-browsing hypothesis and the climate
prostrata, suggesting that they might not play hypothesis individually, it appears to be a
a role in the establishment of the divaricating good candidate for a definitive answer to the
habit itself (Carswell et al. 1996). There are divaricate question.
however too few studies about these growth However, neo-ecological studies alone
regulators to formulate general conclusions are unlikely to entirely resolve the origin of
about their potential effects in controlling the divaricate plants. One way still left to explore
expression of the divaricate habit. was suggested by Cooper et al. (1993):
using molecular phylogenetics to date the
Conclusions divergences between divaricates and their
closest non-divaricate relatives. Past studies
The terms divaricate or divaricating
estimating the age of New Zealand plant
have been variously applied to around 80
lineages (e.g. reviewed by Wallis & Jorge
New Zealand species that we regard as
2018; Heenan & McGlone 2019) have not
occupying a spectrum from truly divaricate
focused on dating such divergences. Such
(small and widely-spaced leaves; wide-angle
studies, and studies on overseas groups that
branching; tough, wiry, tightly interlaced
include New Zealand representative, can still
stems) to semi-divaricate (plants that
offer isolated dates even though they might
present some but not all of these traits). This
not have sampled the closest non-divaricate
spectrum of architectural forms, which we
relative to the divaricate species they included
call divaricating habits, is the expression of
(Appendix 3). The divergence dates between
a phenomenon called the divaricate habit.
congeneric divaricate and non-divaricate
Heteroblastic divaricate species have a
species give us a first hint that the divaricate
divaricate (or semi-divaricate) juvenile form
habit may have appeared less than 10 Mya in
and a non-divaricate adult form, in contrast
most cases. Table 2 provides the theoretical
to the generally smaller (< 8 m) homoblastic
divergence dates one might expect from
divaricates that retain the divaricate form
a study specifically dating splits between
throughout their entire lives. Finally, we
divaricate and non-divaricate species under
coin the term divaricate-like to describe
the different hypotheses in play: the dates of
overseas instances of the divaricate habit
the divergences in Appendix 3 hardly favour
phenomenon, which acknowledges their
one hypothesis over the other, suggesting the
resemblances with New Zealand divaricates
need for a dating effort specifically targeting
while stressing their peculiarities. We hope
divaricate species and their closest non-
that adoption of these terms will help reduce
divaricate relatives, as suggested by Cooper
ambiguities in future research and facilitate
et al. (1993).
clear communication. Our recommendationsYou can also read
