All of the studies have defined QRS fragmen- tation using ECGs obtained during acute MI and mostly within 48 hours of hospitalization (Table 2).

The rate of QRS fragmentation ranged between 20% and 61% and was 38.5 % in total.

In the STEMI population, fQRS was detected in 568 of 1527 patients (37.2%) and in NSTEMI population, fQRS was detected in 327 of 939 patients (34.8%) which was not statistically different (P = 0.41).


All of the studies except for Sheng et al. reported left ventricular EF in study groups.

In six studies, left ventricular EF was lower in fQRS (+) (ranged between 35% and 45%) compared to fQRS (-) group (ranged between 43% and 50%).

9, 14-18 Whereas, three studies reported an insignificant difference of left ventricular EF between the groups.

10-12 Seven studies reporting left ventricular EF in mean ± standard deviation were analyzed with the random effects approach.

The overall effect showed that patients who had fQRS on admission ECG had a significantly lower LVEF than patients without fQRS (WMD −6.01, 95% CI [−9.08, −2.94], P < 0.00001) (Fig. 3)


In six studies the frequency of 3-vessel disease was reported. 10, 12, 14, 16-18 In four studies, the frequency of 3-vessel disease was higher in fQRS (+) group (ranged between 42% and 61%) compared to fQRS (-) group (ranged between 15% and 33%).

In total, the frequency of 3-vessel disease was 46.4% in fQRS (+) group and was 24.2% in fQRS (-) group (P < 0.01).Whereas, two studies re- ported an insignificant difference between groups regarding multivessel involvement.

12, 17 Most of the patients with STEMI were treated with primary percutaneous coronary intervention (77.6%).


Six studies reported in-hospital mortality 13-18 and six studies reported long-term adverse events.

9mortality rates but reported the outcome as MACE only.


Regarding in-hospital events, mortality was significantly higher in fQRS (+) group (99/733; 13.5%) compared to fQRS (-) group (47/1293; 3.6%) (OR 4.03; 95% CI, 1.81-8.94; P = 0.0006) (Fig. 4).

When only STEMI studies were included in the analysis, mortality was higher in fQRS (+) group (57/479; 11.9%) compared to fQRS (-) group (21/814; 2.6%) (OR 6.01; 95% CI, 2.37-15.23; P = 0.0002).

14-16, 18


Five studies reported mortality rates during a follow up period ranging between 6.6 and 28.2 months.

10-12, 16, 17 The mortality rate was higher in fQRS (+) group (89/473; 18.8%) compared to fQRS (-) group (54/1009; 5.3%) (OR 3.93; 95% CI, 1.92-8.05; P = 0.0002) (Fig. 5).

In addition the frequency of MACE was higher in fQRS (+) group (46.9%) compared to fQRS (-) group (14.6%) (OR 5.13; 95% CI, 2.77-9.51; P < 0.00001) (Fig. 6).

When only 3 NSTEMI studies are included in the analysis, mortality rate was higher in fQRS (+) group (17.7%) compared to fQRS (-) group (5.7%) (OR 3.42; 95% CI, 2.01-5.82; P < 0.00001).

10, 12, 17 When 2 studies which required persistence of fQRS(+) throughout the hospitalization period were excluded, 10, 14 presence of fQRS was still found to be correlated with higher risk of mortality in the remaining study population (OR 3.59; 95% CI, 1.99-6.47; P < 0.00001), in STEMI subgroup (OR 8.08; 95% CI, 2.65-24.65; P < 0.00001), 15, 16, 18 and in NSTEMI subgroup (OR 3.20; 95% CI, 1.46- 6.99; P < 0.00001).

12, 17


presence of fQRS is associated with higher risk of in-hospital and long-term mortality and adverse cardiovascular events in patients with AMI.


This is the first meta-analysis focused on STEMI and NSTEMI.

Two prior meta-analyses included patients with stable/unstable CAD, cardiomyopa- thy and ICD implantation.

19, 20 AMI is the most severe form of CAD which is associated with high risk of left ventricular failure, arrhyth- mias and mortality compared to stable patients.

Fragmentation of QRS has been shown to be correlated with myocardial scar, left ventricular dysfunction and arrhythmias in patients with various cardiovascular diseases.

2, 19 In fact, AMI is the initial event in most of patients that lead to heart failure, arrhythmias and ICD implantation.

Determination of QRS fragmentation during the acute phase of AMI (especially within 48 hours) is feasible and as we have shown in this meta- analysis, presence of fQRS may have clinical value in establishing patients with higher risk for short and long term adverse cardiac events.


In this analysis, we have found that presence of fQRS is correlated with short- and long-term adverse cardiac event regardless of the AMI type.

In addition, a higher portion of patients with fQRS had multivessel disease which may result in incomplete revascularization.

We have found that patients with fQRS (+) have lower LVEF compared to fQRS (-) patients.

This finding is concordant with previous reports which found lower LVEF, and larger left ventricular systolic and diastolic dimensions and volumes in patients with fQRS and CAD.

21, 25 As we included only AMI patients, we can assume that appearance of QRS fragmentation even in the early phase of AMI may indicate larger infarct size and worse LV systolic function.

This correlation may partially explain the worse prognosis in patients with fQRS (+).


The prognostic value of QRS fragmentation during the acute phase of ACS was first proposed by Das et al. 26 In that study, they have reported that fQRS had higher sensitivity for diagnosis of STEMI or NSTEMI compared to Q waves, T-wave inversion or ST-segment depression.

In addition, they have found higher long-term mortality rates in fQRS(+) group compared to fQRS (-) group.

This study was not included in this meta-analysis because the mortality and morbidity rates were not reported in the AMI subgroup.

In another study, Pietrasik et al. reported incidence of QRS fragmentation as 53% in AMI patients after 2 months.

8 They found that presence of QRS fragmentation and/or Q waves was not associated with long term adverse events.

Interestingly, they found that patients with resolved Q waves and persistent fQRS had the highest risk for long-term adverse events.


An important confounding factor in evaluation of QRS fragmentation in CAD patients is the timing of the ECG and persistence of QRS fragmentation throughout the study period.

The studies are heterogeneous and persistence of ECG findings were not reported in all studies.

In this meta- analysis, five studies reported data regarding dura- tion of QRS fragmentation 10, 11, 13, 14, 18 In subgroup analysis, we have found that documentation of QRS fragmentation within 48 hours of hospitalization is adequate and is correlated with worse outcome in STEMI and NSTEMI patients.

The data regarding the rate of persistence of QRS fragmentation after AMI is controversial, thus, to our opinion use of the ECGs obtained within 48 hours of hospitalization is adequate for risk stratification of patients.


The exact mechanism of fQRS on ECG has not been fully elucidated in the literature but most of the studies have concluded the main causative mechanism is cardiac fibrosis and scar- ring.

Presence of QRS fragmentation is accepted as a sensitive marker of myocardial scar after AMI.

2 Myocardial damage causes heterogeneity of my- ocardial segments and a conduction delay around the infarction zone or scar accounts for the reason for fragmentation in QRS.

Even if arrhythmic complications were not reported in detail in this analysis, sudden cardiac death is a major cause of death in patients with CAD and MI.

Thus, presence of fQRS may be correlated with arrhythmic compli- cations and SCD that leads to higher mortality risk.


Several potential limitations of present meta- analysis should be taken into account.

First, there is publication bias on considering only published studies.

In addition, language was restricted to English.

About half of the studies were retrospec- tive which warrants more large scale randomized controlled trials.

The duration of follow-up was not same for all studies.

In addition, it is hard to evalu- ate the additive prognostic value of QRS fragmen- tation besides reduced LVEF in patients with AMI.


Presence of fQRS on admission ECG was a predictor of mortality, MACE, deterioration of LV function and presence of multivessel disease in patients with STEMI and NSTEMI.

Further evaluation of clinical use of QRS fragmentation in patients with AMI are needed to establish the risk of arrhythmic complications and mortality in patients with fQRS.


Dear Editor,


We read with great interest the article by G€ung€or et al. [ 1] in the recent issue of your journal.

In this meta-analysis, the authors showed that presence of fQRS was a predictor of mortality, major adverse cardiovascular events (MACE), deterioration of left ventricle function, and presence of multivessel disease in patients with ST-segment elevation myocardial infarction (STEMI) and non-STEMI (NSTEMI).

We would like to add some comments and contributions to this article.


Development of fQRS is a dynamic process and appears approximately 24–48 hours after the onset of symptoms or after diagnosis and following MI necrosis [2].

Therefore, in the majority of studies, the 48th hour were investigated for the definition of fQRS.

Whereas the importance of the presence of on admission fQRS was investigated in two of the studies included in this meta-analysis [3], [4], in others the importance of the presence of fQRS in the 48th hour electrocardiography (ECG) was investigated.

The authors proposed that fQRS within 48 hours of hospitalization is adequate and correlated with worse outcome in the discussion section.

However, in the conclusion section, they indicated that fQRS on admission ECG was a predictor of mortality, MACE, deterioration of LV function, and presence of a multivessel disease in patients with MI.

Stating as fQRS on admission ECG in the conclusion section of the meta-analysis can cause confusion and misperception on the part of the reader, because the fQRS on admission ECG can disappear within the 48 hour follow-up.

For this reason, we think that it will be more correct to say fQRS developing within 48 hours.


In addition, most researchers have recently focused on the number of fQRS derivations pattern rather than fQRS presence.

In our recent study [5], we showed that number of leads with fQRS on ECG is an independent predictor of in-hospital mortality in acute STEMI patients.

Findings related to the number of fQRS derivations are also discussed in three of the studies included in this meta-analysis [3], [6], [7], and it was shown that as the number of fQRS derivations increased, the incidence of MACE and number of vessels with critical stenosis increased; conversely LV function decreased significantly [3], [6], [7].

The concept of at least two derivations is mentioned for the traditional definition of fQRS, but these studies show that the presence of fQRS in even one derivation can be significant.

It can make an additional contribution to this meta-analysis for the authors to investigate findings related to the number of fQRS derivations in the studies included in this meta-analysis.


In conclusion, despite increasing studies, the matter of when the presence of fQRS in surface ECG should be checked and the significance of fQRS in a single derivation are still an area open to discussion.

We believe that instead of the traditionally defined at least two derivations concept, the presence of fQRS in a single derivation is also important and that it will be more meaningful to look at the fQRS developing within 48 hours.

Further meta-analyses and perhaps a guide on fQRS are necessary in order for the shortcomings in this area to be eliminated and for a consensus to be reached.


We would like to thank authors for their interest and positive contributions to our current article [1].

We agree with the authors that, even though in three studies investigating admission electrocardiograms (ECGs) also showed increased rates of adverse events in patients with fragmented QRS (fQRS), our meta-analysis mainly implicates the clinical use of ECGs recorded within the 48 hours of hospitalization [2][3][4].


The prognostic importance of fQRS and its correlation with myocardial scar formation and long-term adverse events have been investigated in patients with coronary artery disease and heart failure.

As we have shown in our meta-analysis, and also in previous studies, the presence of fQRS is associated with more severe form of coronary atherosclerosis and left ventricular systolic dysfunction [5].

As noted by Tanrıverdi et al., the total number of leads with fQRS is correlated with the risk of adverse events [6][7].

But in these studies, the prognostic value of presence of only one lead with fQRS was not reported.

For standardization of the meta-analysis method, we have included only studies which defined QRS fragmentation according to Das, Khan, Jacob, Kumar, and Mahenthiran [8] which necessitates presence of fQRS in at least two contiguous leads.


Thus, from the published data it is not possible to investigate whether the presence of only one ECG lead with fQRS has prognostic value in this meta-analysis.

It is well known that, acute myocardial infarction causes dynamic ECG changes compared to stable coronary artery disease patients.

Serial ECG recordings become an important issue for analyzing the timing of appearance and disappearance of QRS fragmentation.

In most of the studies, the timing of first ECG with fQRS and the disappearance of fQRS (if happened) were not reported in detail.

Only in five studies the rate of fQRS persistence beyond 48 hours was reported and the rate of fQRS persistence was widely different between the studies.

Thus, further studies are needed to clarify the importance of the presence of fQRS in a single lead.


Recent experimental and clinical studies have demonstrated that changes in subchondral bone and a crosstalk between subchondral bone and cartilage play an important role in the development of OA, 9 although the pathophysiology and changes in subchondral bone have not been fully elucidated.

In the early phase, increased osteoclast activity, elevated bone remodelling and hypomineralisation can be found, 7 9 while in later stages low bone turnover and densification of the bone ('bone sclerosis') can be observed.

Addi- tionally, bone marrow lesions (BML) can be detected on MRI.

5 9 Thus, theoretically, the use of antios- teoporotic drugs that can be regarded as antiresorptive drugs (BPs such as alen- dronate, risedronate, zoledronic acid, but also denosumab, a monoclonal antibody against receptor activator of nuclear factor kappa-Β ligand (RANKL)) might have effects on subchondral bone, particularly in the phase of elevated bone remodelling and hypomineralisation.

Indeed, for rise- dronate a reduction in the urinary excre- tion of crboxy-terminal telepeptides of type II collagen (CTX II), usually regarded as a marker of cartilage breakdown, was found, but not on symptoms and/or radio- logical progression.

10 For alendronate and strontium ranelate, a reduction in osteophytes and disc-space narrowing of the spine was found in a post-hoc anal- ysis of studies with patients with osteo- porosis.

11 12 Additionally, in a small study with zoledronic acid, a reduction in BMLs was found.

13 With another antiosteopo- rotic drug, strontiumranelate, which is not a pure antiresorptive drug, a reduction in joint space width was demonstrated in a 3-year trial versus placebo.

14 There are remaining questions how a primary effect on subchondral bone might have subsequent effects on cartilage metab- olism, and on anatomical structural abnor- malities such as disc-space narrowing, osteophytes and BMLs.

Nevertheless, all these data point in the direction that BPs might have an effect on OA (progression).


Since denosumab is also an antiresorp- tive drug, it is plausible that it also might have favourable effects in OA.


Neogi et al used the The Health Improve- ment Network (THIN) database, in which data are collected by general practi- tioners in UK.

Only patients with incident knee-OA were enrolled, and 2006 patients who initiated BPs at least 1 year after diag- nosis of knee-OA were compared with 2006 propensity-matched 'non-BP initia- tors'.

After a mean follow-up of 3 years, the crude incidence of KR was 22.0 per 1000 person-years among the initiators, vs 29.1 among the non-initiators, with an HR of 0.76 (95% CI 0.59 to 0.93).

Obvi- ously, the key question is whether this is a direct effect of BPs on the osteoarthritic joint, or might confounding by indication play a role? For example, do BP users have a more healthy lifestyle, or higher vitamin D levels, or a higher socioeconomic status, or less frailty, and so on?


Without doubt, the authors tried to minimise the effect of confounding by indication, by performing a propen- sity score-matched cohort study, and by sensitivity analysis for those without data on BMI, smoking and/or alcohol, which all support the protective effect of BPs.

Even the potentially lower mortality risk for patients with BP use was calculated.

Nevertheless, although these all seem to be optimal and robust, it is not possible to completely rule out the risk of bias, because unknown bias cannot be detected and thus not calculated.


Remarkably, this year Fu et al 15 published a more or less comparable, nationwide, study from Taiwan. They observed more than 12 000 BP users and 123 000 non-users, all with knee-OA, and they found a 24% reduction in the percentage of patients for KR (HR 0.75, 95% CI 0.69 to 0.83), which is remarkably in line with the THIN data.

The study from Taiwan is larger, which is reflected in the smaller CI. But the authors found also a dose- effect relation: in those individuals who used BPs for more than 2 years and with a medication possession ratio >80%, the risk reduction for a KR was even larger: HR 0.66 (95% CI 0.43 to 0.95).

More- over, the authors observed over a 5-year follow-up period a significantly greater reduction in the use of non-steroidal anti-inflammatory drugs, acetaminophen and glucosamine in the BP users versus the non-users (P<0.001).


what are the consequences? editorial with each other, which is very important because these data validate each other.

Since both studies suggest that BPs reduce the percentage of patients with knee-OA who need a KR with around 25%, this might indicate that patients with knee- OA who also have osteoporosis and an elevated fracture risk should prefer- ably be treated with a BP.

It is too early to conclude that BPs should also be prescribed in patients with knee-OA without osteoporosis, since prospective data on randomised studies in patients with knee-OA in which reduction in patients with KRs who are BP users versus placebo are lacking.


It is important to realise that both studies have the same case-control design, so it cannot completely be ruled out that they may have both the same structural limitation of confounding by indication in its design.

Nevertheless, the larger reduc- tion in KRs in patients with greater expo- sure to BPs is a strong argument in favour of a drug-induced effect.


What would be the next step? Given the paucity of therapeutic options in OA, these data strongly suggest that BPs have a favourable effect on the natural course of OA, which might have important conse- quences for our patients and for societies, since reduction or postponing of KRs might have large financial consequences.

In my opinion, the data should preferably be confirmed in a randomised controlled trial in which elderly patients with inci- dent knee-OA should be randomised to a BP (or another antiresorptive drug, such as denosumab) versus placebo.

Because of the placebo arm, patients with high frac- ture risk resulting from generalised oste- oporosis should be excluded, for ethical reasons.

As a consequence, it could be that patients with osteoporotic subchon- dral bone will be excluded.

However, a large sample size and long study duration will be necessary, unless we are able to select patients with OA with osteochon- dral bone that is vulnerable to the posi- tive effects of BPs, thus with a high bone turnover and some hypomineralisation.

Unfortunately, reliable, quantitative and validated measurements are even with new techniques as dual x ray absorptiom- etry (DXA), CT scan and/or MRI not yet possible.


To summarise, two comparable and high-quality studies have documented and suggested that BP use is associated with a 25% reduction in KRs.

Since KR is a clin- ically relevant and hard endpoint, these studies hopefully might stimulate further research in the role of subchondral bone in OA, which is still urgently needed given the paucity of therapeutic options in OA.


None declared.


provenance and peer review Commissioned; externally peer reviewed.


© Article author(s) (or their employer(s) unless otherwise stated in the text of the article) 2018.

All rights reserved.

No commercial use is permitted unless otherwise expressly granted.


I read with interest your article regarding the potential of bisphosphonates for osteoarthritis (OA) [1].

Since OA affects the entire joint, it is unsurprising that there has been great difficulty developing an effective targeted treatment.

The lifetime risk of symptomatic knee OA has been estimated to be as high as 44.7% [3], and therefore, we are in urgent need of finding a disease-modifying OA drug.


Basic calcium phosphate (BCP) crystals have been found in 100% of OA knee and hip cartilages removed at joint replacement and therefore might represent a potential therapeutic target in OA [4].

BCP crystals include various calcium phosphates, including partially carbonate-substituted hydroxyapatite, octacalcium phosphate, tricalcium phosphate and magnesium whitlockite [5].

BCP crystals have multiple biologic effects in vitro.

They have the ability to stimulate prostaglandins, cytokines and matrix metalloproteinase synthesis in various cells including macrophages, synovial fibroblasts and chondrocytes [6].

BCP crystals also contribute to inflammation in OA via the innate immune system.


Bisphosphonates are well-known analogues of endogenous pyrophosphate.

They have a strong affinity for bone mineral and therefore tightly bind to hydroxyapatite crystals [7].

This may be the reason behind the potential therapeutic effect of bisphosphonates in knee OA.


With OA being the most prevalent rheumatic disease, affecting millions of patients worldwide, it is essential we urgently find a treatment for this much neglected disease.

There is ample evidence that BCP crystals are a pathogenic mediator of OA and bisphosphonates as a potential OA treatment should be explored further.


I read with great interest the letter from Murphy and McCarthy [1]: ‘knee osteoarthritis and bisphosphonates: could BCP crystals be the missing link?’ [ 1]. I recently gave comments on two case-control studies [2], in which the need for a total knee prosthesis was around 25% lower in bisphosphonate (BP) users than in controls [3][4]. What could be the explanation? It could be related to epidemiology: BP-users have a healthier lifestyle than non-users, by doing more exercise therapy, preventing overweight and so on.

The other option is a biological effect, for example, an effect of BPs on the underlying subchondral bone in patients with osteoarthritis (OA) [5].


Murphy and McCarthy bring in that BPs have a strong affinity for basic crystal phosphates (BCPs) and that this might inhibit inflammatory reactions in the synovial fluid [1].

They argued that BCPs have been found in the cartilage of 100% of patients with OA at the time of joint replacement and that BCPs might contribute to inflammation in OA.

Although this is certainly a valuable suggestion, the incidence of clinically manifest knee-osteoarthritis based on BCP-crystals is low in patients with OA.


Since knee-OA is a whole joint disease, cartilage, bone, synovial inflammation and muscular weakness all play a role [6], it is very likely that other factors are among the mean determinants of inflammation and pain in patients with knee-OA.

So, BCP-crystals are probably not ‘the’ missing link, but might be a ‘missing link’.

Nevertheless, since the pathogenesis of OA is not fully elucidated and therapeutic options are scarce, further research in the direction of BCPs and BPs in patients with knee-OA is very welcome.


The genus Wetzeliella and related forms constitute an important group of Paleogene dinoflagellate cysts that have proven to be important biostratigraphic and paleoecological markers.

However, debate and confu- sion over their taxonomy and classification have ham- pered their full utility in these applications, a situation that we aim to address herein.


When Alfred Eisenack (1938) erected Wetzeliella, he did not provide a detailed description for the genus.

He remedied this situation in 1954 by specifying the presence of horns, spines (which, in current dinoflagel- late-cyst terminology, we would refer to as processes) and a capsule (or endocyst) as diagnostic features.

Once the morphology of Wetzeliella was clearly eluci- dated, the number of species assigned to the genus rapidly increased, as did the number of allied genera.

Those genera currently considered to be related to Wetzeliella are Apectodinium, Axiodinium, Charlesdow- niea, Dracodinium, Kisselevia, Rhombodinium, Talla- dinium and Wilsonidium.


The first suprageneric treatment of Wetzeliella and its allies was by Vozzhennikova (1965), who erected the family Wetzeliellaceae and included in it Dracodi- nium, Palaeohystrichophora, Rhombodinium and Wet- zeliella.

Bujak & Davies (1983) proposed the subfamily Wetzelielloideae, within the family Deflandreaceae.

In the subfamily, Bujak & Davies included Apectodinium, Dracodinium, Gochtodinium, Kisselevia, Rhombo- dinium, Wetzeliella and Wilsonidium.

In their diagnosis of the subfamily Wetzelielloideae, Bujak & Davies (1983, p. 135) stated that 'a quadra second intercalary Downloaded by [G. Raquel Guerstein] at 12:44 13 July 2015 plate. .

.forms the I (2a) archeopyle'.


In an extensive revision of dinoflagellates in general, Fensome et al. ( 1993, p. 137) placed the subfamily Wetzelielloideae in the family Peridiniaceae, providing the following diag- nosis: 'Peridiniaceans in which the mid-dorsal anterior intercalary plate is quadra (i.e. four-sided)'.

Thus, as currently recognised, the subfamily Wetzelielloideae is characterised by a quadra 2a plate that touches the third apical plate (3') anteriorly, the first (1a) and third (3a) anterior intercalary plates laterally and the consistently six-sided fourth precingular plate (4") posteriorly (Figure 1).

Other fossil subfamilies of the Peridiniaceae, such as the Deflandreoideae, are characterised by a six- sided (hexa) 2a plate.


Determining which features to use in diagnosing genera within the Wetzelielloideae has been a conten- tious issue, the result being that generic definitions have become blurred.

In our view, this is in large part because of overemphasis on horn development and wall structure at both generic and specific levels.

This situation has in turn led to the decreased utility of wet- zelielloidean taxa as biostratigraphic markers: for example, based on current literature records, Wetzel- iella articulata now spans most of the Eocene and Differentiation of wetzelielloidean archeopyle types is not a new concept: several others, including Bujak (1979), Costa & Downie (1979) and Michoux (1988), have recognised differences in the quadra 2a archeo- pyle.

However, no one has yet tried to define all genera in the subfamily using the archeopyle as the main crite- rion.

Bujak (1979) erected the genus Gochtodinium to accommodate taxa with a distinctive soleiform archeo- pyle (see History of study) and proposed the restriction of Rhombodinium to forms with a soleiform archeopyle and lack of processes, but did not define any other wet- zelielloidean genera according to their archeopyle type.


In this paper, we undertake a major review of all wetzelielloidean taxa and propose several new taxa.

Our proposed hierarchy of morphologic features for distinguishing genera gives priority to archeopyle type, especially the periarcheopyle.

Within groups united by having a distinctive archeopyle type, we use pericystal ornamentation as a secondary criterion in separating genera.

The only deviation from these general princi- ples is in the case of Apectodinium and Axiodinium; both genera have a similar style of archeopyle and peri- cystal ornament, but can be differentiated on the basis of pericoel development and wall thickness.


Although wetzelielloideans are an extinct cyst- based group to which 'para' terminology might be applied, we consider that their paratabulation is a direct reflection of the tabulation, and hence, for sim- plicity, we use thecal terminology.


In his paper erecting the genus Wetzeliella, Eisenack (1938) illustrated two specimens, one of Wetzeliella articulata and the other of Wetzeliella clathrata.

He provided only minimal information on the morphology of the genus and the two species, noting that 'The bris- tled integument and strengthened, almost limb-like protrusions of the body are characteristics of the spe- cies [Wetzeliella articulata]' (Eisenack 1938, p. 187, translation).

Eisenack (1954) designated Wetzeliella articulata as the type of Wetzeliella and indicated that diagnostic features of the genus include the presence of horns (typically one apical, two lateral, two antapical), orna- mentation in the form of 'bristles or spines' (i.e. pro- cesses) and a 'capsule' (i.e. endocyst).

In his description of Wetzeliella articulata, Eisenack (1954) recognised the occasional presence of a 'slip hole' (i.e. archeopyle).

In one specimen, he noted that the operculum remained attached along the upper (anterior) margin of the archeopyle and was folded back.

Eisenack also stated that the archeopyle (in the pericyst) had a quad- ratic outline.

In other, more elongate specimens, arche- opyles were relatively common.

He stated:


I have studied over 100 specimens [of Wetzeliella artic- ulata], of which very few show an opening, as illus- trated in [Eisenack 1954] pl. 7, fig. 6.

In a second specimen, the cover is still connected to the upper part of the opening, as a membranous fragment and is folded upward. . . .

[ T]he cover separates from the shell along a circular seam (sometimes this seam is quadran- gular with rounded corners), but remains connected along its upper margin, i.e. closely below the apex and flaps upward in similar fashion to a tongue.

[ Eisenack 1954, p. 57, in translation]


In today's terminology, Eisenack was describing a clas- sic soleiform archeopyle as described by Bujak (1979, p. 309).

The attached and soleiform nature of the oper- culum was confirmed by one of us (RAF in 1993) in a re-examination of the holotype of Wetzeliella articulata.

Gocht (1955) used a lack of processes and horn development to distinguish Rhombodinium and Draco- dinium, respectively, from Wetzeliella.

Williams & Downie (1966, p. 195), by transferring the type of Dra- codinium to Wetzeliella, subsequently synonymised Dracodinium with Wetzeliella, citing a continuum of horn development among specimens observed in the London Clay.

Gocht (1969) presented a superbly illus- trated review of the species then assigned to Wetzel- iella, and preferred to redesignate Rhombodinium as a subgenus of Wetzeliella.

He attempted to distinguish taxa on the presence or absence of horns and processes but admitted to having only limited success, invariably finding intermediate forms later.


The name Kisselovia was proposed by Vozzhenni- kova (1963) for forms that she described in part as fol- lows: 'Test smooth or has reticulate pattern with spinules in nodal positions, or without them' (transla- tion modified from Stover & Evitt 1978, p. 110).

The generic name Kisselovia, however, was not validly pub- lished in 1963 due to lack of a validly published species name.

Vozzhennikova (1967, p. 103) validated the name, as Kisselevia, by providing a description for the type.

There has been confusion about the correct spell- ing of this generic name, compounded by the addi- tional spelling Kisseljovia, used by Vozzhennikova (1961, p. 1462) À see Fensome & Williams 2004, p. 380À381.

In the present paper, for consistency, we cite the correct name, Kisselevia, except in direct quotes and synonymy lists.


Lentin & Williams (1976) emended Wetzeliella and Kisselevia, and proposed a new genus, Wilsonidium, for forms with predominantly sutural ornamentation on the pericyst.

According to these authors, Kisselevia is distinguished from Wetzeliella by its possession of dis- tally interconnected processes.

Lentin & Williams included in Kisselevia not only those species with cylin- drical trabecula (e.g. Kisselevia tenuivirgula), but also those with a membranous ectophragm (e.g. Kisselevia coleothrypta).

Costa & Downie (1976) reviewed the stratigraphic distribution of Wetzeliella, developed a zonation based on these fossils for northwestern Europe and proposed Wetzeliella subgenus Apectodinium.

The sub- genus Apectodinium was raised to the generic rank by Lentin & Williams (1977).


The first comprehensive review of organic-walled fossil dinoflagellate genera, including wetzelielloideans, was by Stover & Evitt (1978).

These authors accepted Dracodinium as a junior synonym of Wetzeliella, and included in the group Rhombodinium, Kisselevia and Wilsonidium.

In the following year, Bujak (1979) erected the genus Gochtodinium and emended Rhombodinium, both on the basis of the recognition of the soleiform archeopyle type (see Figure 2).


Although mistakenly describing the wetzelielloid- ean archeopyle as hexagonal, Costa & Downie (1979) made a significant contribution by recognising four archeopyle types.

These were the Apectodinium, Wetzel- iella meckelfeldensis, Wetzeliella articulata and Draco- dinium types (see Archeopyle variability).

However, they did not propose generic emendations based on their concepts.

They also undertook an extensive mor- phometric analysis of wetzelielloidean taxa.

Measure- ments included: pericyst length and breadth, endocyst length and breadth, lengths of apical, cingular and antapical horns, length and breadth of periarcheopyle, length from apex to anterior margin of periarcheopyle and length from tip of apical horn to cingulum.

Although lengths and widths of pericysts and endo- cysts were surprisingly consistent, wide variations in horn length were observed within a single species.


Costa & Downie concluded that a few morphometric traits could be used to characterise taxa, such as the smaller size of Apectodinium and the greater width to length ratio in Dracodinium. But they admitted that 'the separation of a number of species was based on the arbitrary division of a continuum' (Costa & Downie 1979, p. 35).


In a phylogenetically oriented review of fossil peri- dinioids, Bujak & Davies (1983) emended the diagnosis for the subfamily to include reference to the quadra second anterior intercalary plate.

Evitt (1985, p. 195À198) included the Wetzeliella and Apectodinium complexes in his 'Pq-cysts' (essen- tially wetzelielloideans).

He noted that most Pq-cysts are over 100 mm long, with a peridinioid outline and cingular horns.

Process development is variable, with common ectophragmal development.

The endocyst, except in Apectodinium, is usually distinct.

Archeopyle formation is exclusively through loss of the 2a plate, which may remain attached anteriorly.

Evitt also noted that where ventral tabulation is discernible, it is of a 'para' type, with 1' contacting 2'' and 6''.

He consid- ered important features for identifying taxa in this group to be outline, number and prominence of horns, cavation, shape of endocyst, process type, presence of ectophragm, tabulation (as paratabulation), difference between peri- and endoarcheopyles and, whether the operculum is adnate.

Michoux (1988) expanded on the ideas of Costa & Downie (1979) by recognising seven distinctive archeopyle types (see Archeopyle variability).

How- ever, although his was an outstanding study in which six new species were recognised, Michoux proposed neither new genera nor emendations of generic diagno- ses or descriptions.


In re-examining the type of Kisselevia, Lentin & Vozzhennikova (1989) restricted that genus to forms that they interpreted as having a reticulate periphragm.

Therefore, they proposed a new genus, Charlesdowniea, for those species with trabecula supported by processes arising from the periphragm as well as those with a membranous ectophragm (such as the type, Charles- downiea coleothrypta).

Lentin & Vozzhennikova (1989, p. 216) stated that: Lentin & Williams (1976) emended the genus Kisselovia to include species from the genus Wetzeliella in which the processes are intratabular and connected distally by trabeculae or solid pieces of ectophragm.

This emendation was based on an erroneous interpretation of the morphology of the holotype, complemented by the morphology of the species they chose to include in the genus.

Unfortunately, Lentin & Vozzhennikova (1989) were unable to re-illustrate the holotype of the type, which is lost, but they did propose a lectotype for Kisselevia ornata.


Since 1989, further progress has been made in our understanding of the wetzelielloideans, largely driven by the realisation that these taxa are ideal index fossils if the main critera for distinguishing genera were primarily the archeopyle and secondarily the nature of the ornament.

The present authors demon- strated this in Fensome et al. ( 2009), when they erected the genera Axiodinium and Talladinium and emended the diagnoses of Apectodinium, Rhombodi- nium and Wetzeliella.


The focus on using the archeopyle as the primary basis for generic differentiation further led us (in Fensome et al. 2009) to restrict Wetzeliella to forms with a soleiform archeopyle.

Thus, many of the spe- cies formerly included in that genus were transferred to Axiodinium.

Applying a similar reasoning to Charlesdowniea, Fensome et al. ( 2009) restricted that genus to forms with an equiepeliform archeopyle, transferring those species with a soleiform archeopyle to the new genus Talladinium.

But these authors did not emend the generic diagnosis for Charlesdowniea. Like Charlesdowniea (as emended here), Talladinium has intratabular processes connected distally by membranes.


In this paper, we expand on the concepts that we presented in Fensome et al. ( 2009) by proposing to dif- ferentiate all the wetzelielloidean genera, apart from Apectodinium and Axiodinium, primarily on archeopyle type and secondarily on ornamentation.

( Apectodinium and Axiodinium both have an equiepeliform archeopyle and distally free processes; however, they are distin- guished by wall structure.) We believe that by adopting such an approach, we are developing a more natural classification based on evolutionary variations in the shape of the 2a plate and on how this influences other aspects of the morphology, such as horn length. And, by following this approach, we are also enhancing the stratigraphic utility of wetzelielloideans.


Wetzeliella and its allies exhibit a distinctive variant of the standard peridinioid tabulation that clearly places it within the family Peridiniaceae (Fensome et al. 1993).

Members of the subfamily Wetzelielloideae are distin- guished by a unique combination of a bipesioid anterior dorsal tabulation and a four-sided ('quadra') 2a plate (Fensome et al. 1993; Figure 1).

The term 'quadra' was first applied to the tabulation pattern of wetzelielloid dinoflagellates by Lentin & Williams (1976).


The signifi- cance of the quadra archeopyle as a distinguishing char- acteristic of this group was also noted by Evitt (1978), who emphasised the need for careful interpretation of the archeopyle, given its relationship to tabulation.

As Evitt so elegantly noted, to state that the 2a plate is hexa or quadra does not necessarily specify the precise shape of the archeopyle.

Often, the only way to demon- strate whether the 2a is hexa or quadra is to compare the widths of the archeopyle with the width of the fourth precingular plate (4 00 ).

If 4 00 is demonstrably wider, 2a is quadra.

Where 4 00 is demonstrably nar- rower, 2a is hexa.

Perhaps there is some merit in follow- ing Evitt (1978), who proposed the descriptive phrases 'archeopyle formed by paraplate 2a in a hexa style para- tabulation' (for hexa 2a archeopyle), or 'archeopyle intercalary in cyst with quadra style paratabulation' (for archeopyle quadra intercalary), but it makes for a cum- bersome description.


The main features used to distinguish genera and species among the Wetzelielloideae have been surface ornamentation, wall relationships and structure, over- all shape (including related horn and pericoel develop- ment) and process morphology and distribution.

With few exceptions, the detailed morphology of the archeo- pyle has not been used to distinguish genera or species.

However, the exceptions deserve comment here.


In the description of one of his new species, Wetzeliella luna- ris, Gocht (1969) noted and illustrated the difference in size between the endo- and periarcheopyle.

Whereas the cingular margins of the two archeopyles coincided, there was a marked difference anteriorly.

The rounding of the anterior margin of the endoarcheopyle was char- acteristic in Wetzeliella lunaris and some other species.

Surprisingly, the two opercula detach as one and remain attached to each other.

Significantly, Gocht (1969) separated Wetzeliella lunaris and Wetzeliella articulata in part on their arche- opyle shape.


This was the first time that variations in archeopyle type had been proposed as a means of sepa- rating species of Wetzeliella.

Gocht's insight was fur- ther demonstrated in his description of Wetzeliella meckelfeldensis.

Based on archeopyle type, he allied Wetzeliella meckelfeldensis with Wetzeliella lunaris but G. Williams et al. Downloaded by [G. Raquel Guerstein] at 12:44 13 July 2015 distinguished the former from Wetzeliella symmetrica, which had a smaller archeopyle, with the periarcheo- pyle being approximately the same size as the endoarcheopyle.


Gocht (1969) also noted that archeo- pyle openings are uncommon in Wetzeliella symmetr- ica.

We consider that this reflects a soleiform archeopyle, with the opercula often falling back in place, like a flap.

Bujak (1979) was first to name a distinctive quadra 2a archeopyle type: the soleiform archeopyle.

In the soleiform type, the peri- and endoperculum remain attached along the anterior margin, usually have a dis- tinctive tongue-like outline and tend to be of the same size.


It is remarkable that the anterior attachment of the operculum was first noted by Eisenack (1954), yet its significance was overlooked for 25 years.


Another milestone paper on wetzelielloidean arche- opyle variation was that by Costa & Downie (1979).

These authors recognised four archeopyle types: the Apectodinium type, in which the peri- and endopercu- lum are attached to each other; the Wetzeliella meckel- feldensis type, in which the periarcheopyle is longer than the endoarcheopyle; the Wetzeliella articulata type, in which the periarcheopyle and endoarcheopyle are of equal length; and the Dracodinium type, in which the periarcheopyle is longer and narrower than the endoarcheopyle.


The idea that the archeopyle may be of fundamen- tal importance to the classification of the wetzelielloid- eans was discussed by Goodman (1983) and Michoux (1988).

Goodman (1983) recognised three basic 2a archeopyle types in the wetzelielloideans: the subcircu- lar, the quadrate and the soleiform.

The subcircular type is another term for the Apectodinium type of Costa & Downie (1979).

Goodman (1983) subdivided the quadrate type into the quadrangular, the broad quadrangular and the trapezoidal.

Separation of these three types is based on the variations in the height/ width ratio of the archeopyle.

Michoux (1988) consid- ered the quadrangular to be equivalent to the Wetzel- iella articulata type of Costa & Downie (1979), the broad quadrangular to be equivalent to the Draco- dinium archeopyle type of Costa & Downie (1979), and the trapezoidal to be equivalent to the Wetzeliella meckelfeldensis type of Costa & Downie (1979).

Good- man (1983) retained Bujak's (1979) concept for the sol- eiform archeopyle type.


In part, Michoux (1988) followed the classification of Costa & Downie (1979).

He retained the Apecto- dinium, Wetzeliella articulata and Wetzeliella meckel- feldensis archeopyle types, changed the name of the Dracodinium type to the Wetzeliella solida type (since he included that species in Wetzeliella), and added the rectangular, soleiform and uncinata types.


According to Michoux, the Apectodinium type has a subcircular to ovoidal outline with the endo- and perioperculum being of similar size and shape, and free.

In the Wetzel- iella articulata type, the endo- and periarcheopyle are of similar size and shape and both opercula are free: the outline is quadrangular with rounded corners, and narrows anteriorly.

In Wetzeliella meckelfeldensis, the periarcheopyle and endoarcheopyle are the same width, but the periarcheopyle extends further anteri- orly and narrows considerably.


Although Michoux renamed the Dracodinium type as the Wetzeliella solida type, he did not change the concept.

This archeopyle type has a laterally elongate endo- and periarcheopyle, with the former sometimes wider than the latter.

The broad lateral dimension of the archeopyle tends be present in forms with a relatively short and indistinct apical horn, a co-occurrence that is probably not coin- cidental.

Both the peri- and endooperculum are free.


The three remaining archeopyle types defined in Michoux (1988) are the soleiform type, the rectangular type and the Wetzeliella uncinata type.

The soleiform type is as defined by Bujak (1979) and hinges (pun intended!) on the anterior attachment of the peri- and endoperculum.

Although not mentioned by Michoux, this type is characteristic of the holotype of Wetzeliella articulata.

By naming another archeopyle type the Wetzeliella articulata type, Michoux inadvertently cre- ated some ambiguity.

However, his reasoning was understandable in the sense that, when one reviews the literature, many of the forms included in Wetzeliella articulata do have a tapered rectangular 2a with a detached operculum.

Uncertainty arises because the type of Wetzeliella articulata does not have this morphology.


Michoux's rectangular archeopyle type, as in Wil- sonidium (now Castellodinium) compactum, is charac- terised by 'subparallel opposite sides and rounded corners' (Michoux 1988, p. 21).

Although Michoux noted that in this type, the archeopyle suture runs all the way around the periphery of the 2a plate, he found that in most specimens, the opercula remained adher- ent.

In this paper, we consider the archeopyle of Wilso- nidium (now Castellodinium) compactum an early example of the soleiform archeopyle.


One of the most distinctive 2a archeopyle types is encompassed by Michoux's Wetzeliella uncinata type (Plate 4, figures 15À20).

In this variant, the periarcheo- pyle tapers anteriorly and is elongate, the opening in part being in the apical pericoel.

Thus, the periarcheo- pyle in this case is considerably longer than the endoarcheopyle.

One notable feature is that the peri- operculum is adnate along its anterior margin, but the endoperculum is free.


Although one of the pioneers in understanding the complexity and variability of the quadra 2a plate and the archeopyle that forms from it, Michoux considered Palynology Downloaded by [G. Raquel Guerstein] at 12:44 13 July 2015 archeopyle variation to be an intrageneric feature.

Based on observations of thousands of specimens over a number of years, we have concluded that the archeo- pyle is of fundamental importance to understanding the phylogeny and to refining the stratigraphic distri- bution of the wetzelielloideans, and hence should form the basis of the taxonomy of the group.

That this has not been the case in the past has led to the extending of ranges of many species to the point where they are not useful stratigraphically.

An example is Wetzeliella articulata.

This name has been applied to all forms with five horns (one apical, two lateral and two antapi- cal, usually of unequal length) and nontabular distribu- tion of processes that are distally free, regardless of archeopyle type.

Restriction of Wetzeliella articulata to forms with a soleiform archeopyle, as in the holotype, has the potential to constrain its range and thus make it far more useful stratigraphically.


The stratigraphic significance of an attached quadra 2a has been supported by the observations of other authors.

For example, Lentin & Vozzhennikova (1989, p. 220) noted: 'There has been a great deal of discussion among palynologists regarding the relative significance of the soleiform archeopyle. . . .

However, our experience suggests that the attachment of the 2a paraplate along its anterior margin is stratigraphically controlled À even within the same species'.

These authors reported an increasing percentage of soleiform archeopyles from the Early to Late Eocene, citing Rhombodinium longimanum as an example.

It would be helpful to know the Early Eocene records to which Lentin & Vozzhennikova (1989) referred.

From our data, the oldest Eocene record of a taxon with a solei- form archeopyle is Wilsonidium compactum, which was recorded by Michoux (1988) from the early Lutetian nannoplankton zone NP 16.


Although acknowledging an increase in occurrence of the soleiform archeopyle in the late Eocene and early Oligocene, Lentin & Vozzhennikova (1989, p. 220) stated that they considered 'the presence or absence of a soleiform archeopyle to be an intraspecific variation, and do not accept its presence or absence as a basis for the separation of genera'.

They thus considered Goch- todinium to be a junior synonym of Wetzeliella.

It turns out that, in our view, Lentin & Vozzhennikova were correct in their synonymy but for the wrong reason.

However, at that time, the nature of the archeopyle in the holotype of Wetzeliella articulata was not acknowl- edged to be soleiform.


The classification of wetzelielloideans is confused by the array of variable features and the lack of a con- sistently applied hierarchy among those features on which to base a phylogenetic framework.

This situa- tion led Goodman (1983, 1985) to advance ideas on character discordance.

He noted (1985, unnumbered page) that the 'solution to date in dealing with this variation has been fundamentally to propose a new genus for each new combination of characters.

The result has been an overclassification of the complex at the generic level. . .'.

At the time, Goodman wrote that there were approximately 70 species in the 'Wetzeliella complex' (i.e. what we would now call the Wetzeliel- loideae), distributed among seven genera.

In our view, restricting the number of genera in a family or sub- family is valid only if the generic differentiations are unworkable.


4. Proposed parameters for classification Fensome et al. ( 1993, p. vii) stated that 'below the rank of class, amphiesmal structure, especially tabulation, is the most valuable and meaningful criterion in classify- ing dinoflagellates. . .'.

A major drawback in applying this principle to the wetzelielloideans is that the tabula- tion is so consistently quadra bipesioid.

However, var- iations occur in the nature of the archeopyle in both the pericyst and the endocyst.

Since these variations reflect differences in shape and relative dimensions of the 2a plate, and based on our studies of these dinofla- gellate cysts, we feel that this aspect of tabulation can be used effectively and meaningfully to subdivide the subfamily Wetzelielloideae into genera.

We consider that other approaches to classification of the wetzeliel- loideans, emphasising other morphological features at generic rank, have proven impractical and should no longer be used.


In this paper we recognise several archeopyle types and use these as diagnostic criteria for genera within the Wetzelielloideae (Figures 2 and 3).

We define these archeopyle types on the basis of overall shape and attachment.

Archeopyles with opercula that are attached at the anterior margin are termed 'soleiform', following Bujak (1979), or 'hypersoleiform'.

These two terms are defined as follows: We use the term 'epeliform' to denote an archeopyle with a detached operculum.

We also apply epeliform as a suffix for more specific types defined on the basis of shape and relative proportions of the archeopyle margins, as follows: To use the archeopyle type alone in defining genera within the subfamily Wetzelielloideae would lead to some large genera that are diverse in ways other than archeopyle type.

Therefore, we use the nature and distri- bution of ornamentation (primarily process develop- ment) and wall relationships (e.g. development of ectophragm) to distinguish genera with the same archeo- pyle type.

For example, we have subdivided forms with a soleiform archeopyle on the basis of the following: Two variables in wetzelielloidians that are often over- looked because they are difficult to quantify are the development of the ambital pericoel and the thickness of the endophragm.

Through the Eocene, there is a general trend for the ambital pericoel to be reduced and the endophragm to become thinner; for example, compare species of Dracodinium with species of Wetzel- iella.

The width of the ambital pericoel has a direct relationship to the categorisation of the archeopyle in some genera, particularly those with latiepeliform archeopyles.

One such genus is Dracodinium, in which the periarcheopyle often markedly extends into the api- cal pericoel.

Another is Petalodinium, in which the spe- cies Petalodinium sheppeyense commonly has an archeopyle that opens primarily into the apical peri- coel.

We have not used the above criteria in generic dif- ferentiations, but such variations can provide clues to the age of species and assemblages.


A notable exception to the age-related variability in the features mentioned in the previous paragraph is the genus Apectodinium.

Although Apectodinium first appears in the Selandian and does not occur in any great abundance above the Ypresian, it consistently has a thin endophragm and a pericyst and endocyst that are appressed.

This distinctive feature is what dis- tinguishes the genus from Axiodinium, which is charac- terised by an ambital pericoel and usually, but not always, a thicker endophragm.


We use horn development for species differentia- tion.

However, determining which antapical horn is the longer can be difficult; indeed, Iakovleva & Heilmann- Clausen (2007) recently noted that in the species Epeli- dinium (as Wilsonidium) pechoricum, the right antapical horn is longer than the left.

This situation can be seen also in scanning electron micrographs of specimens illustrated herein (Plate 5, figures 1 and 3).

Variation in pericyst ornamentation is also a critical factor when speciating.

However, in our view, the relative length and development of horns and pericyst ornamention are secondary to archeopyle type for generic separation in wetzelielloideans.

Thus, forms with a membranous or reticulate ectophragm that have been included within a single species or genus may now be separated from one another at the generic level on the basis of their archeopyle type.

This approach makes the classification of the group more logical and increases its value in stratigraphic determinations, which is one of the pri- mary considerations when erecting species.


In the systematics section that follows, genera are pre- sented in alphabetical order.

In contrast and to facili- tate comparison, the plates are arranged so that all forms with the same archeopyle type are generally together.

The diagnoses are intended to outline as briefly as possible the morphological features that dis- tinguish each genus.

The descriptions provide a detailed account of the degree of variability in all mor- phological features.

The asterisk indicates the species containing the type of the genus ('type species').

In Appendices 1À3, we provide lists of taxa and affilia- tions relating the names used herein with those cited in Fensome & Williams (2004).


The plates include many images from the extensive slide collection of the senior author (GLW), and include his own photographs and those gleaned from G. Williams et al. Downloaded by [G. Raquel Guerstein] at 12:44 13 July 2015 many colleagues over the decades, most notably Lew Stover.

Unfortunately, details such as size and prove- nance have been lost for many of these specimens; but we have decided to use the images anyway because col- lectively they provide an excellent insight into the mor- phology of wetzelielloids, especially the archeopyle.

To give a more specific idea of the sizes of taxa, we include some information available from the literature (from protologues of the appropriate species unless otherwise specified) as a final paragraph in the Discussion of each genus.

For overall dimensions in generic descrip- tions, we follow Stover & Evitt (1978, p. 5) in using the terms 'small' (less than 50 mm), 'intermediate' (50À100 mm) and 'large' (greater than 100 mm) A 'thin' wall is interpreted as being about 1 mm.


Note that in the plates the designation 'sp.' does not indicate that we recognise a specific informal taxon, but that we can assign the specimen illustrated only to generic rank.

Thus, the labelling of multiple specimens within a genus as 'sp.' implies neither that they are con- specific nor that they are mutually separate forms.


The generic names Axiodinium and Talladinium were introduced by the present authors in Fensome et al. ( 2009) and so, technically, their authorship should be cited as "Williams, Damassa, Fensome & Guerstein in Fensome et al 2009." However, for brevity, we cite the authorship as "Williams et al. in Fensome et al. 2009." Similar considerations apply also to some other taxo- nomic citations throughout the systematic section.


Wilsonidium may be distinguished from other genera having hyperepeliform archeopyles as fol- lows: Rhadinodinium has a pericyst that is smooth or ornamented only with features of low relief.

Sageno- dinium has trabeculate processes.

Stenodinium has pro- cesses that are distally free.

Other genera with penitabular to sutural ornamentation are Castellodinium, Dolichodi- nium, Stichodinium and Vallodinium.

Castellodinium has a soleiform archeopyle, Dolichodinium has a hypersolei- form archeopyle, Stichodinium has a latiepeliform archeo- pyle and Vallodinium has an equiepeliform archeopyle.


The holotype of Wilsonidium tabulatum has a peri- cyst length of 149 mm, a pericyst width of 138 mm, and endocyst 83 by 85 mm.

The holotype of Wilsonidium ornatum has a pericyst length of 156 mm, a pericyst width of 151 mm, an endocyst length of 99 mm and an endocyst width of 102 mm.

Discussion.

Fensome & Williams (2004) retained this species in Wilsonidium.

However, the morphology appears to conform with Spinidinium rather than any wetzelielloidean genus; hence, we retain the species as Spinidinium rugosum.


The genus typically occurs in the Middle Eocene (Lutetian), but probably extends into the Late Eocene or even the Early Oligocene.


Early Eocene (Ypresian).


Early Eocene (Ypresian) to Middle Eocene (? early Lutetian).


Talladinium? angulosum (Châteauneuf & Gruas-Cav- agnetto 1978) comb.

nov., stat.

nov.


Numerous studies have acknowledged the importance of wetzelielloidean taxa in delineating ages within the late Paleocene to Oligocene (Figures 4aÀb), although ranges must be treated with caution as species were commonly not constrained by the archeopyle morphol- ogy of their holotypes.


In a pioneering study, Wilson G. Williams et al. Downloaded by [G. Raquel Guerstein] at 12:44 13 July 2015 (1967) recognised the usefulness of Wetzeliella in refin- ing stratigraphic control in the PaleoceneÀEocene strata of New Zealand.


Of the eleven species he recorded, seven were restricted to individual New Zea- land regional stages and three occurred in two stages.


One of the species that Wilson identified was Wetze- liella (now Charlesdowniea) coleothrypta.


The only spe- cies that did not appear to be useful stratigraphically was Wetzeliella articulata.


Caro (1973) was first to propose a zonation based primarily on Wetzeliella.


In a study of Paleo- ceneÀlower Eocene strata of the Spanish Pyrenees, Caro named five zones, which are shown in Figure 4a.


According to Caro, the zones were total range zones, with the nominative species being restricted to its zone.


A comparison of the data of Wilson (1967) and Caro (1973) prompts interesting questions.

Why, for example, is the total range of Wetzeliella articulata restricted to the earliest middle Ilerdian (a regional early Eocene stage) in Caro's scheme, whereas according to Wilson the species has no stratigraphic value?

A plausible explanation, if one uses the archeopyle type for the initial separation, is that specimens identified as Wetzeliella articulata by many authors represent several species.

Another possibility is that ranges of many species in the Northern and Southern hemispheres are different, rendering it difficult to compare zonations.


A second question is whether the specimens identi- fied as Wetzeliella coleothrypta by the two authors repre- sent the same species.

The specimen illustrated in Wilson (1967, figs. 12À14) appears assignable to Charlesdowniea columna, whereas the specimen that Caro illustrated (1973, his pl. 5, fig. 8) agrees with our concept of Charles- downiea coleothrypta.

But Caro also illustrated a speci- men that he assigned to Wetzeliella clathrata (his pl. 5, fig. 7), which appears, like Wilson's specimen, to be assignable to Charlesdowniea columna (now Piladinium).


Jan du Chêne et al. ( 1975) identified five dinoflagel- late-cyst associations in the ThanetianÀLutetian of Haute-Savoie, France, three of which were named after wetzelielloidean species.

One diagnostic wetzelielloi- dean dinoflagellate cyst found only in the youngest À the Areosphaeridium diktyoplokum association À is Wetzeliella (now Rhombodinium) perforata.


A comprehensive zonation based on peridinioid taxa, mainly species of Wetzeliella, is that of Costa & Downie (1976).

These authors proposed a zonation for the PaleoceneÀOligocene strata of northwestern Europe, which was applicable in southern England, Belgium, northern Germany and the Paris Basin and keyed to the nannofossil zonation.

Eight of the nine zones in the scheme proposed by Costa & Downie (1976, text-fig.

5) were named for wetzelielloidean spe- cies (Figure 4a).


Châteauneuf & Gruas Cavagnetto (1978; Figure 4a) proposed a fourteenfold zonation extending from the late Thanetian to the Rupelian in the Paris Basin.

All fourteen zones were named for wetzelielloid- ean taxa, many of which had been noted as having stratigraphically restricted ranges by Costa & Downie (1976).

In their text-figure 2, Châteauneuf & Gruas Cavagnetto (1978) showed what they regarded as morphologic variations and stages of evolution in four of the taxa: we pursue this hypothesis in the next section.


Costa & Downie (1979) reiterated the value of the Wetzelielloideae (which they referred to as the Wetzel- iellaceae) in biostratigraphy.

In their text-fig.

3, they plotted the stratigraphic range of 42 species, which they variously assigned to the genera Apectodinium, Kisselevia, Wetzeliella, Dracodinium and Rhombodi- nium.

One example is Kisselevia (now Sophismatia) ten- uivirgula, which extends from nannofossil zones NP 12 to NP 20.

Unfortunately, Costa & Downie (1979) did not reference their data sources.


Wilson (1984) proposed a dinoflagellate-cyst zona- tion for the Late Jurassic to Eocene of New Zealand.

One of the Paleocene and most of the Eocene zones were named after species of the Wetzelielloideae.

Wil- son (1988; Figure 4a) proposed a minor modification of the Early Eocene zonation, with the uppermost zone being named after the areoligeracean species Membra- nophoridium perforatum.

Most of the zones named after wetzelielloidean species represent the total range of the index species.

Exceptions are: the Apectodinium homomorphum Zone, whose top is based on the FAD (First Appearance Datum) of Wetzeliella cf.

hyper- acantha (Wilson 1988, named this taxon Wetzeliella spinulosa); the Charlesdowniea (as Kisselevia) edwardsii Zone, whose base is marked by the LAD (Last Appear- ance Datum) of Charlesdowniea coleothrypta and whose top is marked by the LAD of the index species; and the Stichodinium (as Wilsonidium) lineidentatum Zone, whose base is defined by the LAD of Castellodi- nium (as Wilsonidium) echinosuturatum and whose top is defined by the FAD of Wetzeliella hampdenensis.


The archeopyles in most of the wetzelielloidean spe- cies after which the zones of Wilson (1984) are named fit with our observed trends relating to changes in archeopyle type through time.

One possible exception is Wetzeliella? spinulosa, which may have a soleiform archeopyle.

Wilson (1988), when erecting the species, stated that the 'operculum [is] sometimes attached along the anterior margin, generally free'.

The shape of the archeopyle cannot be determined from the illustrated specimens.

But an attached operculum would be a first for an Early Eocene wetzelielloidean dinoflagellate cyst.

Another exception is Vallodinium? echinosuturatum.

In the line drawing of Wilson (1967, fig. 3b), the shape of Palynology Downloaded by [G. Raquel Guerstein] at 12:44 13 July 2015 the 2a plate is epeliform. But in several illustrations (e.g. Wilson 1967, figs. 22À25; Wilson 1988, pl. 25, fig. 3b and pl. 26, fig. 1c); the operculum seems to remain in place.

Thus, Vallodinium? echinosuturatum may have an attached epeliform operculum.


Williams & Bujak (1985), in a review of dinoflagel- late-cyst zonations, plotted the stratigraphic ranges of 21 wetzelielloidean species.

Some of their stratigraphic information is erroneous: an example is the FAD of Charlesdowniea (as Kisselevia) edwardsii and Rhadino- dinium (as Dracodinium) politum at 63.7 Ma in the Danian.

Williams & Bujak indicated the range of Wet- zeliella articulata to be from 54.25 to 36.2 Ma, which is less than the range of 53.2 to 30.4 Ma for Charles- downiea (as Kisselevia) coleothrypta.

However, the sequence of the individual ranges does show a consis- tency that is close to the present view, with the general order of appearances of the genera being Apectodinium, Wetzeliella (if one includes species now assigned to Axiodinium), Dracodinium and Rhombodinium.

No spe- cies of Wilsonidium were included in the plots of Williams & Bujak (1985).


Several papers presenting Paleogene zonations based primarily on wetzelielloidean species have been published by Russian authors.

Andreeva-Grigorovich (1991) published an elevenfold zonation for the late Tha- netian to early Rupelian of the former USSR, with the index taxa including species of Apectodinium, Wetzeliella, Kisselevia, Dracodinium and Rhombodinium (Figure 4a).

The general ordering is similar to that in Costa & Downie (1976) but with less control in the Ypresian.

Andreeva et al. ( 2011) provided a slightly modified ver- sion of this zonation for the late Thanetian to Rupelian of the Ukraine, but retained the same 11 zones.

Powell (1992; Figure 4b) proposed a formal zonation for the Paleogene of Britain and adjacent areas that was based in large part on wetzelielloideans.

Of the 27 zones,


Downloaded by [G. Raquel Guerstein] at 12:44 13 July 2015 12 were named after species of this group.

Powell illus- trated some of the wetzelielloidean species that he used as zonal index markers.

Where it can be seen, the archeo- pyle type shown in these illustrations accords with our concepts.

The exception, however, is Wetzeliella articu- lata, which Powell did not use as an index species.

The specimen he illustrated (Powell 1992, pl. 4.6, fig. 10) has an equiepeliform archeopyle, rather than a soleiform archeopyle.

Our redefining of wetzelielloidean taxa according to archeopyle type restricts some stratigraphic ranges in Powell (1992).

For example, Powell gives a range for Wetzeliella articulata as extending from the early Ypresian into the Rupelian.

Although precise ranges for our new configurations of species remain to be refined, the morphology represented by the type of Wetzeliella articulata does not extend below the late mid- dle Eocene and is likely restricted to Bartonian through Rupelian strata.

Other species also significacntly restricted because of the new morphological understand- ing are Wetzeliella (now Stenodinium) meckelfeldensis, Charlesdowniea coleothrypta, Charlesdowniea (now Sophismatia) reticulata and probably Wetzeliella ovalis.


Bujak (1994, fig. 1; also Bujak & Mudge 1994, fig. 2; see Figure 4b herein) presented a dinoflagellate cyst zonation for the latest Paleocene and Eocene of the North Sea in which he erected nine zones and 23 sub- zones.

The one zone named after a wetzelielloidean was the oldest, the Apectodinium augustum Zone.

How- ever, he named five subzones after wetzelielloideans.

In the accompanying events chart, Bujak also included the LADs of Dracodinium simile (frequent occurrence), Dracodinium (now Petalodinium) condylos (consistent), Dracodinium varielongitudum (common), Dracodinium (now Rhadinodinium) politum (consistent), Draco- dinium varielongitudum (consistent), Dracodinium pachydermum (now a junior taxonomic synonym of Axiodinium eoceanicum) (common), Rhombodinium (now Petalodinium) rhomboideum and Wetzeliella ovalis.

Since Bujak (1994) did not illustrate any of the wetzelielloidean species, it is not possible to determine archeopyle types.


Williams et al. ( 1998), using the Paleogene time scale of Berggren et al. ( 1995), gave two sets of values for dinoflagellate cyst stratigraphic ranges.

The first was for northwestern Europe, the second was for the Mediterranean area.

These authors recorded 24 species and one subspecies of wetzelielloidean taxa from northwestern Europe, but only 7 species from the Med- iterranean area.

Most of the species, especially those of Apectodinium, appeared earlier in the Mediterranean than in northwestern Europe but this was not always the case.

For example, Rhombodinium porosum had its Mediterranean FAD at 37.00 Ma whereas its FAD for northwestern Europe was 37.34 Ma.

The exclusion of data regarding the stratigraphic range of Wetzeliella articulata reflects that Williams et al. ( 1998) had reser- vations about its stratigraphic range.

Williams et al. ( 1999) also gave ages in a similar format to that of Williams et al. ( 1998), and with the same control.

The oldest wetzelielloidean taxa were four species of Apectodinium, which had late Thane- tian LADs that ranged from 56.42 to 55.86 Ma.

The first species of Wetzeliella, Wetzeliella (now Sophisma- tia) meckelfeldensis, had a FAD of 53.94 Ma, margin- ally older than Dracodinium waipaweaense and Charlesdowniea reticulata, both at 53.82 Ma.

Thus within a very short interval of time the three genera, which we would now refer to as Sophismatia, Petalodi- nium and Stenodinium, had made their first appearan- ces.

This means that the equiepeliform (Sophismatia) was soon joined by the latiepeliform (Petalodinium) and hyperepeliform (Stenodinium) archeopyle types.

The equiepeliforms had earlier been represented by Apectodinium only.


Determining when the soleiform archeopyle first appeared is not easy from the ranges provided by Williams et al. ( 1999).

If Wetzeliella? spinulosa, described by Wilson (1988) from the Waiwapan Stage (Early Eocene) of New Zealand, does indeed have a soleiform archeopyle, then its FAD would be within the Ypresian.

Otherwise, the FAD of Rhombodinium draco is given as 39.39 Ma, which is within the Barto- nian.

Wetzeliella articulata was given an FAD of 49.73 Ma, but this reflects the broad definition of this species as used at that time.


According to Williams et al. ( 1999), and probably in reality, Dracodinium is restricted to the Ypresian.

The biggest surprise is the stratigraphic range of Charlesdowniea, which according to Williams et al. ( 1999) is 53.82 Ma (FAD of Charlesdowniea reticulata) to 37.34 Ma (LAD of Charlesdowniea coleothrypta).

We suspect that the younger records are of morpholog- ically similar forms that have soleiform archeopyles.

If confirmed, such forms would now be included in Talladinium.


Partridge in McGowran et al. ( 2000; Figure 4b) compared the Paleogene dinoflagellate cyst zonations for the Gippsland Basin, southeastern Australia, with that for New Zealand as proposed by Wilson (1984, 1988) and for Antarctica as proposed by Wrenn & Hart (1988).

None of the marker species for the Paleo- gene of Antarctica are wetzelielloideans. But the simi- larity between the Gippsland Basin and the New Zealand zonations is striking, especially the series of events that Partridge recognised for the Wetzelielloid- eae.

The events, which include FADs and LADs, cover the late Paleocene to Early Oligocene and highlight the restricted stratigraphic ranges of many of the species.


Further refinements in our understanding of the stratigraphic ranges of wetzelielloidean species were G. Williams et al. Downloaded by [G. Raquel Guerstein] at 12:44 13 July 2015 provided by Williams et al. ( 2004).

Recognizing the variability in FADs and LADs according to paleolati- tudes, or more correctly also according to control by paleooceanic currents, these authors gave values for five regions: low latitudes, northern- and southern- hemisphere middle latitudes, and northern- and south- ern-hemisphere high latitudes.

Unfortunately, they listed only 14 wetzelielloidean taxa, including one spe- cies of Apectodinium, three of Charlesdowniea, four of Dracodinium, three of Rhombodinium, two of Wetzel- iella and one of Wilsonidium.

The sparse data make it impossible to comment on stratigraphic changes in morphology in the wetzelielloideans.


Recent updates of the stratigraphic ranges of wetze- lielloidean species are published in Powell & Brinkhuis (in Gradstein et al. 2004, fig. 20.3 and in Gradstein et al. 2012, fig. 28.9; with identical information in both publications).

Gradstein et al. ( 2004) provided FADs and/or LADs for 18 wetzelielloidean taxa, which included two species of Apectodinium, three of Charles- downiea, five of Dracodinium, four (and one subspecies) of Wetzeliella and three of Rhombodinium.

The data were based on northwestern European sections.

With such a relatively low number of taxa, important trends are hard to delineate, but there is a definite clustering of Dracodinium species in the Ypresian between 53.6 and 48.7 Ma.

Likewise, Rhombodinium is recorded from the Bartonian to Rupelian.

Charlesdowniea appears in the Ypresian but, since LADs are not given for two of the three species, the overall range of the genus cannot be determined.

Apectodinium is restricted to the late Thane- tianÀYpresian.

The widest range from Ypresian to Chattian is for Wetzeliella. This is not surprising consid- ering the present, in our view confused, records in the literature.


Andreeva-Grigorovich et al. ( 2011; Figure 4b) pro- posed a slightly modified version of the zonation erected by Andreeva-Grigorovich (1991).

The major difference was in the designation of two non-wetzeliel- loidean taxa as index species.


A significant paper on the Paleogene dinoflagellate cysts of western Siberia is that of Iakovleva & Aleksan- dreva (2013; Figure 4b), who proposed 15 zones span- ning the late Thanetian to the mid Priabonian.

Thirteen of the zones are named for wetzelielloidean taxa, and show a logical sequence when the morphol- ogy of the species is considered.

The oldest, as in some other wetzelielloidean-based zonations, is named after Apectodinium hyperacanthum.

Sequentially, this is fol- lowed by Apectodinium (now Axiodinium) augustum, Deflandrea oebisfeldensis, Wetzeliella (now Axiodinium) astra, Wetzeliella (now Stenodinium) meckelfeldensis, Dracodinium simile, Dracodinium varielongitudum, Charlesdowniea coleothrypta, Charlesdowniea (now Pila- dinium) columna, Areosphaeridium diktyoplokum, Dracodinium pachydermum (now considered a taxo- nomic junior synonym of Axiodinium eocaenicum), Rhombodiniu draco, Rhombodinium porosum, Kisselevia ornata and Charlesdownia clathrata subsp.

angulosa (now Talladinium angulosum).

The zonal index species reflect the stratigraphic ranges of the wetzelielloidean archeopyle types, with the oldest being the equiepeli- form and hyperepeliform and the youngest being solei- form.

For example all the index species of the uppermost four zones have soleiform archeopyles.


The problem of establishing evolutionary relationships among fossil dinoflagellates was expressed, perhaps overly pessimistically, by Evitt (1981).

Fensome et al. ( 1993; see also Medlin & Fensome 2013) nevertheless established a broad, evolutionarily based classification for dinoflagellates, including fossils, that has largely withstood the test of time.

Still, trying to establish meaningful phylogenic relationships both within the Wetzelielloideae and between the subfamily and other groups is challenging.

Nevertheless, the difficulty of determining phylogenetic relationships of wetzelielloid- ean taxa has not deterred some from attempting to do so.


The first attempt to propose a phylogenetic tree for wetzelielloideans was that of Châteauneuf & Gruas Cavagnetto (1978, text-figure 2), who considered the root stock to be Apectodinium.

From this root stock the authors postulated the evolution of four taxa - Wetzeliella meckelfeldensis subsp.

lobisca (now Draco- dinium lobiscum), Dracodinium simile, Wetzeliella sym- metrica and Kisselevia (now Sophismatia) tenuivirgula.

Châteauneuf & Gruas Cavagnetto's line drawings of these four taxa show equiepeliform (Wetzeliella meck- elfeldensis subsp.

lobisca and Dracodinium simile), hyperepeliform (Wetzeliella symmetrica) and latiepeli- form (Kisselevia tenuivirgula) archeopyles.

That Wetze- liella symmetrica would have a hyperepeliform archeopyle and be restricted to the late Ypresian to Bartonian does not fit with our interpretation, nor with the middle Oligocene age of the holotype of this species - an age later endorsed by Andreeva-Grigoro- vich (1991), who considered Wetzeliella symmetrica to be a marker species for the early Rupelian.

Thus, the evolutionary sequence postulated by Châteauneuf & Gruas-Cavagnetto (1978) seems questionable.

Costa & Downie (1979) presented a 'morphogenetic chart' for the wetzelielloideans, in part based upon archeopyle type but also on other morpho- logical features and stratigraphic occurrences.

These authors considered Apectodinium to have been the ancestral taxon for the group, evolving from the deflandreoid peridiniacean Spinidinium.

Costa & Downie based this idea on the similarity of the archeo- pyle and the weakly developed pericoel, features that they deemed common to both genera.

However, Spini- dinium has a hexa 2a plate whereas Apectodinium has a quadra 2a plate.

Moreover, Spinidinium commonly exhibits an adnate operculum that remains posteriorly connected to the rest of the cyst, with the 2a joined along the boundary with the 4" plate.


In wetzelielloi- deans with an attached operculum, the attachment is along the anterior margin of the 2a plate, with the 3 0 and 2a plates remaining connected.

Also, such attach- ment does not occur in the earliest wetzelielloideans, but is a consistent feature in taxa occurring in younger, Bartonian-Rupelian rocks.

Recognition of Apectodi- nium as the wetzelielloidean 'root stock' is understand- able if based on its first appearance as early as the Selandian and on its possession of an equiepeliform archeopyle.

Costa & Downie (1979) viewed Apecto- dinium as giving rise to Wetzeliella (now Stenodinium) meckelfeldensis, with its hyperepeliform archeopyle, and thence directly or indirectly to most other wetze- lielloideans within a short interval during the early Ypresian.

Costa & Downie (1979) had major problems deter- mining the affinities of Wilsonidium, which they had correctly determined had a hyperepeliform archeopyle (in our terminology).

They concluded that Wilsonidium derived from Alterbidinium (as Alterbia) pentaradiatum.

Similar caveats apply to this suggestion as to the Apec- todinium-Spinidinium relationship discussed above - indeed Alterbidinium could be thought of as a spineless Spinidinium with the same tendency to have a posteri- orly attached hexa archeopyle/operculum.

Bujak (1979) and Bujak & Davies (1983) also devel- oped significant ideas on wetzelielloidean relationships.

Bujak (1979) emphasised the continuity of the quadra archeopyle in the wetzelielloideans, concluding that it is found only in that group and is thus a diagnostic fea- ture.

However, he expressed uncertainty over the nature of the intercalary archeopyle in Apectodinium.

Bujak & Davies (1983) modified the phylogenetic model of Costa & Downie (1979), primarily by regard- ing Alterbidinium? pentaradiatum subsp.


precedum as the root stock.

These authors reasoned that the quadra 2a plate evolved because of the lateral extension of the cingulum in the wetzelielloideans.

According to Bujak & Davies (1983), one offshoot from Alterbidinium? pen- taradiatum subsp.

precedum gave rise to Wilsonidium, which they regarded as an evolutionary dead end.

Another branch led to Apectodinium, the root stock of all other wetzelielloideans.

Evitt (1985, p. 201) commented that 'It seems prob- able that the . . .

cingular arrangement [seen in Proto- peridinium] occurred throughout the Wetzeliella- Apectodinium complexes . . . .' This would involve only three cingular plates plus a transitional plate, in con- trast to the peridiniacean condition with five or six cin- gular plates plus a transitional.

Evitt gave no direct evidence for this feature and further added '. . . but there is little likelihood that this will be provable in very many instances.' Despite the speculative nature of Evitt's comments, they have been the basis for the widely held belief that the wetzelielloideans are closely related to modern protoperidinioids and thus, by extension, heterotrophic.


In contrast, we view the wet- zelielloids as not being closely related to the protoperi- dinioids.

Scanning electron micrographs presented herein (Plate 5, figs. 4 and 11) suggest at least one and probably two breaks in the cingular plate series on the dorsal surface.

Protoperidinioids have only three cin- gular plates (Fensome et al. 1993), with no sutures on the dorsal surface.

The evidence presented here indi- cates that wetzelielloids have at least four, and possibly five, cingular plates plus a small transitional plate on the ventral surface.

The only significant differences between wetzelielloid and deflandreoid/palaeoperidinioid tabulation are the quadra versus hexa 2a plate and asso- ciated differences in adjacent plates (Figure 1).

This, together with the stability and consistent symmetry of the epicystal tabulation, tentatively allies the wetzeliel- loids with the deflandreoids and palaeoperidinioids.

As the wetzelielloidean archeopyle invariably involves only the 2a plate, its affinity may lie closer to the deflan- dreoids.

But this is speculative, and the origin of the wet- zelielloids among peridiniaceans remains unclear.


That wetzelielloideans are probably not related to protoperidiniaceans also accords with their usual lack of brown pigmentation of the cyst wall, the latter being a feature of protoperidinacean cysts and suggestive of a heterotrophic habit (Mudie 1992).

In extensive stud- ies of Paleogene deep-sea material, one of us (SPD) has rarely encountered wetzelielloids in samples; the reverse would be expected if wetzelielloids were hetero- trophic.

This sparsity of wetzeleilloideans in deeper water deposits accords with the findings of Downie et al. ( 1971), who recognised a Wetzeliella association in the London Clay of southeastern England and pos- tulated that it denoted estuarine conditions.

Thus, there seems substantive evidence that the wetzelielloids preferred shallow-water environments and hence were probably autotrophic rather than heterotrophic.


Modern ideas emphasise evolution's bush-like rather than tree-like nature, and so it follows that the wetzellielloidean fossil record represents isolated branches.

In this context, it is perhaps not advisable to try to connect or place individual species on the overall bush.

However, evolution did occur and morphologies did change over time in ways that we can recognise À the trick is to pick out which morphological features are telling the most meaningful evolutionary story.

Building on the work of Evitt (1985), Fensome et al. ( 1993) concluded that for dinoflagellates as a whole (and especially for fossil forms), changing tabulation was the feature that revealed the most meaningful evo- lutionary story.

Features such as surface ornamenta- tion, horn and process morphology and cavation had their place in defining taxa at lower ranks, but for determining taxa at higher rank and understanding evolutionary trends, tabulation was key.


In the peridiniaceans, the stability of the tabulation makes recognition of evolutionary trends difficult. But if we can relate even subtle changes in, say, archeopyle shape, that reflect changes in tabulation, we may be able to develop a workable model.

Our focus on archeopyle types in the wetzelielloideans gives us a win- dow into changes in the tabulation of this subfamily.

In contrast, variations in horn length and periphragm ornamentation probably reflect environmental controls rather than broader phylogenetic patterns, as has been suggested for other groups of dinoflagellate cysts (e.g. Monteil 1991).

By utilising changing archeopyle form, we can discern the broader evolutionary story.


As Apectodinium, the earliest known wetzelielloid- ean, has an equiepeliform archeopyle type, it seems logical to propose that this type reflects the 'root stock' of the subfamily, developing in the Selandian (Figure 5).

Accepting this, the other archeopyle types evolved very rapidly, since taxa with hyperepeliform, latiepeliform and hypersoleiform types are known from the Ypresian, when 'experimentation' in the group was obviously rife.

Such experimentation fol- lowed by stabilisation has occurred in archeopyle development in other peridiniacians; an example can be found among fossil deflandreoids and palaeoperidi- niods (taken collectively), which show a variety of com- binations of archeopyle types in the Middle to Late Cretaceous (for example, Chichaouadinium and Luxa- dinium); in contrast most Cenozoic members of these two subfamilies have a simple one-plate anterior inter- calary archeopyle.


The latiepeliform archeopyle, which characterises Dracodinium, like the hyperepeliform type, is strati- graphically restricted to the Ypresian and Lutetian.

Forms with the soleiform archeopyle appear in the late Lutetian.

Hyperepeliform types do not fit into the evo- lutionary pattern if Wilson (1967) is right in consider- ing Wilsonidium tabulatum to be late Eocene.

C. Clowes (pers.

comm., 2014) considers this species to be no younger than middle Bartonian, which À although still later than expected À would not be so anomalous.

Latiepeliform types seem not to have survived into the Middle Eocene, though hypersoleiforms did, and per- haps gave rise to the earliest soleiform types in the Lutetian (see Michoux 1988).

However, taxa with this archeopyle type are rare until the Bartonian, when they come to dominate wetzelielloidean assemblages.


At the same time, there is a rapid decline in those taxa with equiepeliform archeopyles, which disappear in the Bartonian.

Thus, by the Priabonian and Rupelian, taxa with soleiform archeopyles don't simply dominate assemblages À they are the only wetzelielloideans pres- ent.

There is much uncertainty over the occurrence of wetzelielloideans in the Chattian but, if present, we would expect them to have soleiform archeopyles.


Why the hypersoleiform and soleiform archeopyle types have opercula that remain attached anteriorly is a mystery.

In peridiniaceans, this anterior attachment is found only in the wetzelielloideans, so perhaps it has some relationship to the distinctive quadra tabulation.

Why the soleiform archeopyle type became dominant is also puzzling; perhaps it somehow offered better pro- tection before and during the initial stages of encyst- ment.

Another mystery is the identity of the non- wetzelielloiodean group that the subfamily evolved from. They are so similar to other fossil peridiniaceans, yet so distinctive in the morphology of their 2a plate, that at present, any ideas would be pure speculation.


Archeopyle type shows a significant relationship to apical horn length.

As would be expected, the hypere- peliform and hypersoleiform archeopyles occur only in taxa with long apical horns, whereas in forms with the latiepeliform archeopyle, the apical horn is reduced.

In equiepeliform and soleiform types, the apical horns can vary from short to long.

The lengths of other horns vary considerably in all five archeopyle types, suggest- ing that, as observed in the Phoberocysta-Muderongia group (Monteil 1991), general horn length may be related to environmental parameters.

Also, as shown by Iakovleva & Heilmann-Clausen (2007), the left antapical horn can be reduced, with the right antapical horn being the longer.

Their observations highlight some of the drawbacks in using relative horn length for generic and specific separation.


Pericyst-endocyst relationships also tend to change with time, with circumcavation largely disappearing in the BartonianÀPriabonian.

Endophragm thickness decreased, so that BartonianÀRupelian taxa almost invariably have a thin endophragm.


The peridiniacean subfamily Wetzelielloideae shows considerable morphological variability, particularly in horn development and ornamentation.

The impressive array of wetzelielloidean forms has tended to deflect attention from the more phylogenetically important but less striking morphology of the archeopyle, and this has led to problems with the taxonomy and conse- quent biostratigraphic utility of the group.

Following Fensome et al. ( 1993), we believe that the overriding criterion for generic assignment must be tabulation.

Within the wetzelielloidean complex, the general tabu- lation is strikingly consistent, a tendency for tabulation stability echoed among fossil peridiniaceans as a whole but in contrast to modern peridiniacians (and fossil and modern protoperidiniaceans).


Members of the Wetzelielloideae are unique in pos- sessing a second intercalary (2a) plate that is four-sided (quadra), in contrast to the six- (or, rarely, five-) sided 2a plate of other fossil peridiniaceans.

Unlike many peridiniaceans, only the 2a plate in the wetzeliel- loideans is involved in archeopyle formation.

However, this plate shows variation in shape and relative dimen- sions in the peri- and endoarcheopyle, either of which may have a detached or an attached operculum.

We have used these variations in the archeopyle as the pri- mary morphological features in defining or redefining genera in the Wetzelielloideae, leading us to a proposed new classification (Figure 3).

Based on this concept, we suggest possible relationships of wetzelielloidean gen- era in the form of a cladogram (Figure 6).


We recognise six genera with an equiepeliform archeopyle, five with a soleiform archeopyle, four with a hyperepeliform archeopyle, five with a latiepeliform archeopyle and one with a hypersoleiform archeopyle.

As our understanding of the wetzelielloideans increases, more new genera may fill the morphological gaps that currently exist.


We have used ornamentation type and distribution as secondary features for differentiation at the generic level.

Our proposed scheme with regard to ornamenta- tion in part reflects prior definitions of existing genera.

Wetzeliella is characterised by processes that are dis- tally free, whereas Rhombodinium has ornamentation of low relief and Charlesdowniea has an ectophragm.

Forms like Wilsonidium but with a soleiform archeo- pyle are included in the new genus Castellodinium.

When such variations in ornamentation are related to archeopyle type, and the genera redefined accordingly, it provides a more realistic view of the evolution of the group emerges and, hence, more meaningful and useful stratigraphic ranges.


Our proposed classification is, in itself, an evolution of previous ideas.

Without the pioneering studies of Costa & Downie (1976, 1979), Bujak (1979) and Michoux (1988), we would have struggled to make sense of the wetzelielloideans.

We still have much to learn, but we believe that application of the ideas expressed herein will point the way forward.

We have told the 'hole' story as we presently understand it.

Let us hope that we can build on this story and thereby provide greater insight into the stratigraphic and palae- oenvironmental utilisation of the wetzelielloideans in the Paleogene.


The taxonomic revision of the dinoflagellate cyst subfamily Wetzelielloideae by Williams et al. ( 2015) places primary emphasis on the type of archaeopyle, and secondarily on wall ornamentation.


Williams et al. ( 2015) argues that this provides more clarity for taxonomic differentiation within the subfamily of Wetzelielloideae, and adds to the stratigraphical significance of species within.


We find, however, that their proposed revision (1) introduces taxonomic criteria that divert drastically from these in other dinoflagellate cyst subfamilies, (2) unnecessarily erects and emends many new genera and species, and (3) poses serious practical limitations, which together (4) lead to profound reduction of the stratigraphical applicability of many marker species.


In this contribution, we substantiate our concerns regarding the approach and criteria used by Williams et al. ( 2015).


We propose to retain the generic definitions of Wetzelielloideae that existed prior to the revisions by Williams et al. ( 2015), until a revision supported by the community is available.


Williams et al. ( 2015) have proposed a taxonomic revision of the dinoflagellate cyst subfamily Wetzelielloideae. In their view the ‘generic definitions within the subfamily of Wetzelielloideae have been blurred, and too much focused on wall ornament and horn development’ (Williams et al. 2015, p. 290).

These authors further argue that the blurred generic definitions have ‘limited the utility of Wetzelielloideae as biostratigraphic marker’.

As an example the authors refer to Wetzeliella articulata, a species that has a remarkably long stratigraphical range of 32 million years, from the Paleocene to the Oligocene.


In fact, they assume that the criteria used in this species concept are not satisfactorily distinctive to cover (apparent) morphological variability.

Therefore, they have introduced novel concepts for the taxonomy at the generic level for the Wetzeliellioideae, placing primary emphasis on the type of archaeopyle, and secondarily on wall ornamentation.

Williams et al. ( 2015) argued that the emphasis placed on the archaeopyle type provides much more clarity for taxonomic differentiation within the subfamily Wetzelielloideae.


Williams et al. ( 2015) defined five different types of the 2a intercalary archaeopyle (equiepeliform, hyperepeliform, latiepeliform, soleiform and hypersoleiform).

Further, these authors defined five different types of wall ornamentation, which they applied as a secondary criterion at the generic level.

The authors reviewed all species in the subfamily in terms of archaeopyle type and wall ornamentation, resulting in a matrix.

Their review requires the formal description of no less than 13 new genera, emendation of the diagnosis of three existing genera, and the formal description of three new species.

They concluded that the soleiform archaeopyle is a consistent feature in the younger stratigraphical range (i.e. Bartonian and younger) of the Wetzelielloideae, while the epeliform archaeopyles in this subfamily occur in the older stratigraphical record (Selandian–Bartonian).


We agree with Williams et al. ( 2015) that a thorough review of the taxonomic concepts and definitions for Wetzeliellioideae would benefit the scientific community, and we greatly appreciate the efforts made in this direction.

In theory, the approach taken by Williams et al. ( 2015) could result in a solid, consistent taxonomic framework, since it is based on clear generic criteria.

We also agree that some variability in archaeopyle type and level of detachment exists within the subfamily of Wetzeliellioideae.

After careful consideration, however, we find that their proposed revision (1) introduces taxonomic criteria that divert drastically from well-established conventions, (2) unnecessarily erects and emends many new genera and species, and (3) poses serious analytical and practical limitations, which together (4) lead to a profound reduction of the stratigraphical applicability of marker species, while not introducing any new stratigraphical markers in replacement.

In this contribution, we substantiate our concerns regarding the approach and criteria used by Williams et al. ( 2015) and, based on these concerns, propose to retain the original generic definitions of Wetzelielloideae.


Although in theory the taxonomic revision proposed by Williams et al. ( 2015) provides a clear and consistent set of definitions, we have identified several critical issues in its application that can essentially be narrowed down to four main issues.


Extinct dinoflagellate cyst species cannot be directly linked to the affiliated biological species – even extant motile/cyst relationships are not established fully (e.g. Head 1996) [1].

Therefore, any taxonomic framework for extinct dinoflagellate cysts must rely on clearly visible, distinguishable morphological characteristics.

For this reason, dinoflagellate cyst families are typically separated based on plate tabulation patterns following the system of Fensome et al. ( 1993) [2].


Taxonomic definitions at the generic level are made predominantly based on specific morphological and geometric features (such as cyst outline, cavation, number of wall layers, process outline and distribution, plate and/or sutural ornamentation, etc.), with the archaeopyle type being a consequence of geometry.

Williams et al. ( 2015) broke with this convention because they specifically consider archaeopyle type to be an indicator of phylogeny.

Specifically, Williams et al. ( 2015) applied the basic assumption that the archaeopyle type directly reflects the shape of the plate(s) involved in archaeopyle formation, which is not necessarily the case for all dinoflagellate cyst species (e.g. Harland 1982) [3].