This article is a commentary on Liu et al. (2021).

In their recent review in this journal, Liu et al. (2021) argue that sexual differences in the allocation to reproduction by male and female plants may cause sexual differences in their responses to biotic (e.g. herbivory) and abiotic stress (e.g. moisture stress). Their general argument is that the nett reproductive costs are higher for females because they not only flower but must also produce fruits/cones/seeds (their Figure 3). They suggest (their Figure 2) that females can ameliorate their higher costs of reproduction such as by maximizing resource acquisition and resource gain. Many other previous reviews have also argued for higher female costs (Barrett and Hough 2013; Barrett et al. 2010; Juvany and Munné-Bosch 2015; Obeso 2002). My aims in this commentary are (i) to note that theory predicts equal sexual allocation to reproduction, (ii) to argue that some of examples cited by Liu et al. (2021) do not suggest the theory is incorrect and finally, (iii) to provide a Cape (South Africa) perspective to show that differences in allocation cannot be invoked ad hoc to explain vegetative or other differences between the sexes. Vegetative differences between the sexes must ultimately be related to differences in sexual function, as is the case in animals, and not to differences in nett allocation to reproduction.

There are many reasons why the sexes should allocate equally. Firstly, at the most basic level evolution is about fitness, thus the life of all males and females is ultimately, equally and totally allocated to reproduction. Secondly, in biparental organisms (with limited in-breeding) because the genetic benefits of sex are an almost equal contribution to the genome of the off-spring, theory predicts that the sex ratio should be equal (Hamilton 1967). Also, because the genetic benefits of sexual reproduction are equal, the ‘costs’ or allocation must be equal (or else one sex is cheating). Say males allocated less to reproduction, they would have more resources to allocate to vegetative growth and thus grow larger or live longer, none of which would benefit them unless it ultimately contributed to their fitness via reproduction, in which case this increased vegetative growth is a reproductive allocation. Liu et al. (2021) acknowledge the expectation of sexual equality in allocation but then proceed to use nett allocation differences to explain the interesting differences they noted between the sexes.

In animals there is no clear difference between vegetative and sexual traits. For example, the brain is also a sexual organ needed for mating success and therefore it is meaningless to compare male and female allocation to reproduction, because it must include the lifetime of the entire individual. Male allocation is clearly not limited to the sex organs. It is an illusion that clear differences between vegetative and sexual allocation exist in plants. For example, the architecture of plants must simultaneously serve sexual purposes for pollen dispersal, pollen capture, seed dispersal as well as for vegetative purposes such as capturing light. There are correlations (Corners Rules) between the sizes of leaves, branches and inflorescences and plant architecture (such as degree of branching) which indicate that selection on any one of these traits will affect the others (e.g. Midgley et al. 2019). This makes it difficult to determine whether allocation is to reproduction or not. The size of a branch and its associated hydraulics (such as xylem size) is determined by both its associated flowers and leaves. Also, unlike the case in many animals, the sexes in many plant species cannot avoid competing and thus they need to be competitively equal to prevent distorting sex ratios, especially to male dominated populations. In animals, stark differences between the sexes (e.g. size, colour and ornaments) are explained by factors such as sexual selection, rather than unequal allocation to reproduction. The same explanations should apply to plants.

The argument that the costs of reproduction may differ between the sexes in plants continues because it is difficult to measure, even on subsequent growth, and to quantify across their entire lifetime. For instance, for direct costs there is the issue of which currency to use (which limiting nutrients) and the fact that the sexes allocate differently in time with males typically making an earlier commitment (Obeso 2002). For indirect evidence of the costs of reproductive allocation, such as the impact on size and sex ratios, there too are problems such as the role of natal sex ratios, clonality, age and sex determination effects (e.g. certation).

Liu et al. (2021) cite two references in support of the hypothesis of higher direct costs of reproduction of females and both are problematic. Firstly, Leigh and Nicotra (2003) argued that female allocation was about 10 times that of males in their study taxon. However, they found no differences in size or sex ratios or long-term water use patterns in their study taxa. It is highly unlikely that such large direct allocation differences will have no indirect impacts such as on growth, mortality or have no eco-physiological consequences. Leigh and Nicotra (2003) used biomass as their currency of allocation (not nutrient contents as advised by Obeso 2002) and they measured biomass when fruits were ripe, i.e. when pollen (which has low biomass but high nutrients) had already been shed; these factors may inflate the female contribution. In the second cited paper, Bañuelos et al. (2004) investigated differences in herbivory between the sexes. However, although they found secondary chemistry differences, they found no sexual differences in degree of herbivory and thus this paper does not support the higher costs hypothesis. Liu et al. (2021) state that ‘as discussed in the study of Juvany and Munné-Bosch (2015), higher reproductive investment in females may cause a decrease in the energy invested into growth and defense, thus reducing stress tolerance’. However, two of the papers cited by Juvany and Munné-Bosch (2015) to indicate higher costs of female reproduction, Leigh and Nicotra (2003), as well as Pickering and Arthur (2003) also used the largely discredited biomass allocation methodology rather than nutrient contents. Like Leigh and Nicotra (2003), Pickering and Arthur (2003) also found that the total biomass of male and female plants was similar, suggesting no nett differences in the cost of reproduction. The point here is that the evidence that the direct costs of reproduction differ between the sexes is weak and paradoxically some of the cited papers suggest that there are no indirect costs.

Liu et al. (2021) cite Yule and Burns (2019) who argued that male Aristotelia serrata plants have higher levels of sap herbivory than females and this is because males have more resources than females. If males have extra resources, why then are males not better defended? If females had been more heavily infested by larvae would the ad hoc explanation be that they had fewer resources to allocate to defence? A recent large meta-analysis found no consistent differences in herbivory, chemical defences and the sexes in dioecious plants (Sargent and McKeough 2022). These authors found that as the sample of studies increased the sexual differences dwindled. This is in line with the initial studies focussing on outliers. The same might apply to sex ratios, with initially only unequal sex ratios being seen as interesting. In the Cape (South Africa) dioecious plants are extremely abundant and can dominate entire mountainsides. Despite this abundance there have only been three published measurements of adult sex ratios and one of adult size ratios (Midgley and Cramer 2022) and here ratios were equal. I suggest that the lack of studies is because populations appear to be 1:1 in size and number and are thus considered relatively uninteresting.

Based on Olano et al. (2017), Liu et al. (2021) argue that differences between males and females in water and carbon requirements lead to females being less water stress tolerant than males. Olano et al. (2017) showed anatomical differences between males and females in Juniperus, which they interpreted as being due to higher reproductive allocation by females. However, they provided no field data to verify any nett differences in moisture stress. This is relevant because as noted below, males and females may have different phenology. For example, in the dioecious Cape Restionaceae, water use efficiency (WUE, as measured using δ¹³C) can differ between the sexes with females being less WUE (Araya et al. 2010). This was interpreted ad hoc as the physiological consequence of higher female allocation to reproduction (Araya et al. 2010). van Blerk et al. (2022) using actual water use measurements as well as fine scale δ¹³C measurements between the sexes of a Cape Restionaceae species, showed that these differences were not due to inherent differences in WUE, but were due to the different phenology of male and female culm growth (males grow earlier and allocate more fully to reproduction earlier, when soils are drier). They concluded that earlier growth is more costly to males, but because culms of both sexes reached the same size, there was no nett difference between the sexes. The same phenological difference applies to extremely vegetatively different sexes in Leucadendron rubrum, where female leaves can be up to 10 times larger than males. Harris and Pannell (2010) suggested that females had greater hydraulic efficiency than males and that this was due to greater reproductive costs in cone-bearing females. However, WUE and nett hydraulic differences do not differ between the sexes (Midgley 2010; Roddy et al. 2019). In part this may be because males commit to reproduction and growth early when conditions are dry and hot (November–March) whereas females grow and produce seeds in the cooler, moister period (January–May) (de Kock et al. 1994). Thus, males and females may be different (e.g. vegetatively, phenologically) but that there is no nett difference in resource use and there is no evidence that one sex allocates more to reproduction than the other.

A better direct test for the differences in allocation is whether females in dioecious species produce double the recruits as do co-occurring hermaphrodites. Say males allocate y units to reproduction and females x units. For a dioecious female to have the same fitness with its allocation to reproduction (x + y), compared with two hermaphrodites (2x), would imply that male and female allocation is the same (x + y = 2x). Bruijning et al. (2017) showed no differences in reproductive output and population growth rate (fitness) of dioecious versus hermaphroditic taxa in the large, detailed and long-term Barro Colorado Forest data set. They assumed (and largely found) 1:1 sex ratio and that dioecious females produced double the fruit/seed load of hermaphrodites. This indicates no direct (e.g. fecundity) or indirect (e.g. mortality) costs of female reproduction. It is to be expected that dioecious and hermaphrodite forest species that coexist, must have the same overall fitness and therefore that dioecious females have the same fitness as two hermaphrodites. In the fire-prone Cape fynbos vegetation, most Proteaceae species die in fires and recruit immediately after fires as seedlings and this includes hermaphrodite (e.g. Protea) and dioecious taxa (e.g. Leucadendron, Aulax). They must have the same fitness or else the situation would be unstable (Midgley et al. 2019). In conclusion, we should be sceptical of studies which show, or invoke ad hoc, differences in nett allocation to reproduction between the sexes in plants. It is not expected, impossible to measure and meaningless.

Acknowledgements

I thank Steve Johnson (UKZN), Mike Cramer (UCT) and Joe White (RBGK) for comments.

Conflict of interest statement. The authors declare that they have no conflict of interest.

In the comment, Midgley (2022) stated that our general argument is that ‘the net reproductive costs are higher for females because they not only flower but must also produce fruits/cones/seeds (Figure 3). Midgley (2022) suggests (Figure 2) that females can ameliorate their higher costs of reproduction by maximizing resource acquisition and resource gain’. However, in our review, we summarized the general opinion and pointed out that this pattern was not universal (see more detail in Liu et al. 2021b). In consistent with previous reviews, our review argues that there is no widespread rule in sex-related differences in the cost of reproduction despite the general opinion that females have higher reproductive costs than males (Darwin 1877; Liu et al. 2021b; Lloyd and Webb 1977). We summarized possible factors causing biased sex ratios in plants, rather than only underpinning the higher net reproductive costs in females than in males (Liu et al. 2021b). Similarly, we proposed possible mechanisms causing sexual differences in responses to biotic stress, rather than underpinning the higher net reproductive costs in females than in males (Liu et al. 2021b), which is also adapted from Núñez-Farfán and Valverde (2020).

Despite the widespread view that reproductive costs of plants are higher in females than in males, different results have also been reported in the literature (Delph and Bell 2008; Leigh 2006). In our review, we discussed the relative reproductive costs of the sexes in a specific plant species and condition, but did not compare the absolute reproductive cost of males and females throughout their life history (Liu et al. 2021b). Moreover, we explained that there was no uniform view of the reproductive costs of females and males (Liu et al. 2021b). This is different from the statement that the reproductive cost must be the same in the two sexes (Midgley 2022).

It has been proposed that the estimate of reproductive costs in males and females may differ in their temporal allocation patterns, such that females may possess great compensation mechanisms in the production of fruits (Sánchez-Vilas 2011; Zunzunegui et al. 2006). For example, males may have higher reproductive costs than females during flowering due to the large cost of pollen and flowers, but the reproductive cost of females may be higher than that of males due to the great investment in the production of fruits (Sánchez-Vilas and Retuerto 2011; Zunzunegui et al. 2006). Additionally, females have been suggested to have larger roots in absolute terms, while males allocate more biomass towards roots at later stages of plant growth (Oñate et al. 2012). These studies emphasized the important roles of the absolute and relative sink and source in reproductive costs, and the timing of resource deployment in sexual dimorphism in the annual plant Mercurialis annua (Vilas 2011). Overall, it is important to generate large-scale data about the reproductive investment in females and males, including the roles of multiple interacting factors, taking into account sexual differences in the intensity, frequency and developmental stage of reproductive events (Juvany and Munné-Bosch 2016; Retuerto et al. 2018).

In addition, Midgley (2022) states that ‘the costs of reproduction may differ between the sexes is controversial because it is difficult to measure, and it is also contrary to theory’. Is it this why the author suggested that there was no difference in reproductive costs between females and males? The author cited references from Leigh and Nicotra (2003), and argued that ‘It is highly unlikely that such large direct allocation differences will have no indirect impacts such as on growth, mortality, or have no eco-physiological consequences’. Doust (1989) has proposed that, based on the resource allocation theory, reproduction can directly compete with defense responses and vegetative growth when the resources are limited, which implies that resource allocation is associated with plant species and nutrient traits (Juvany and Munné-Bosch 2016; Liu et al. 2021a, 2021b).

Several studies have indicated that sex-specific functional traits would be strongly affected by environmental factors (Guo et al. 2022; Liu et al. 2021c, 2022a, 2022b; Yu et al. 2020, 2022; Zhang et al. 2021). As discussed above, the observed annual growth rates are indeed equivalent in both sexes, which implies a potential compensation mechanism (Case and Ashman 2005). Therefore, it is possible that there are no indirect impacts on traits, such as growth and mortality, between females and males when the spatial and temporal allocation dynamics, resource availability and diversity of species are taken into account over the whole growing season and even over the whole life-cycle of perennial plant species (Retuerto et al. 2018).

As discussed above, there may be a tradeoff between production, growth and defense in dioecious plant species (Doust 1989; Juvany and Munné-Bosch 2016). The allocation of resources in plants is considered to be affected by many factors, such as plant genotypes and environmental factors (Ackerly 1997; Bazzaz 1997; Liu et al. 2020b; Schultz et al. 2013). The higher resources of males do not represent most of the resources needed to be used for defending as proposed by Midgley (2022). If males have extra resources, why would they need extra resources to defend better? In consistent with previous reviews, there has been no generalization for sexually biased herbivores, which are associated with morphological and physiological traits, reproductive periods, food selection by the herbivores, which need to be clarified in future studies (Barrionuevo et al. 2021; Liu et al. 2021b; Pereira et al. 2020). In our review, we only summarized recent views about sex-specific herbivores and attempted to provide possible explanations according to existing studies (Liu et al. 2021b). Biased sex ratios have been reported to be associated with reproductive costs, mortality, sex choice and sex-specific responses to different environmental conditions (Field et al. 2013; Harris and Pannell 2008; Stehlik and Barrett 2005). Thus, sex ratios in plant populations may reflect species coexistence and resource unitization (Queenborough et al. 2007). At the same time, sex ratios may be biased due to potentially reproductive individuals, which may not be completely censured over several flowering seasons (Queenborough et al. 2007). We do not fully agree with the author’s statement ‘I suggest that the lack of studies is because populations appear to be 1:1 in size and number and are thus considered relatively uninteresting’ by Midgley (2022).

It has been reported that females and males usually exhibit sex-specific responses to abiotic and biotic stresses (Liu et al. 2020a, 2020b, 2021b, 2021d; Retuerto et al. 2018; Zhang et al. 2021). Of course, under certain conditions, there are no sexual differences in certain traits between females and males (Chen et al. 2014; de la Bandera et al. 2008; Varga and Kytöviita 2012). In our previous paper, we summarized that sex-specific differences were greater in response to drought stress, and that the sexes showed slight or little difference under optimal water supply (Chen et al. 2014; Olano et al. 2017). In the study by Olano et al. (2017), the authors selected populations occurring in two contrasting sites, which represented the extremes of the climatic range on the Iberian Peninsula. Therefore, we cannot conclude that there are no field data to verify any net differences in moisture stress, as stated in the comment by Midgley (2022). Moreover, sexually different responses may exist at a particular point of time, but we did not emphasize the existence of absolutely unequal net allocation differences in reproduction (Liu et al. 2021b).

Differences in hydraulic efficiency between plants are largely dependent on the plant species, stress degree and plant growth and development periods (Barbara and Stefan 2009; Gao et al. 2021; Liu et al. 2022b). We did not make the absolute statement about the differences in hydraulic efficiency between females and males in our review (Liu et al. 2021b). In the commentary paper by Midgley (2022), the author argued ‘Also, because the genetic benefits of sexual reproduction are equal, the “costs” or allocation must be equal (or else one sex is cheating)’. We would suggest the author to give some evidence to support his argument. Moreover, we did not use net allocation differences to explain the interesting differences between the sexes. Instead, we reviewed previous studies for possible mechanisms behind sexual differences between the sexes (Liu et al. 2021b).

We noticed that the author acknowledged the difficulty to compare male and female allocation to reproduction (Midgley 2022). However, this does not exclusively mean that the costs of reproduction differ between the sexes. Moreover, we did not suggest that it was meaningless to compare male and female allocation to reproduction (Liu et al. 2021b). Estimates of the sex ratio and cost of reproduction in plant populations have important implications for resource use by animals, reserve design and mechanisms of species coexistence, as well as implications for potential cascading consequences of skewed sex ratios on the structure and stability of ecosystem communities (Hultine et al. 2016; Queenborough et al. 2007). However, these issues have been rarely investigated. In conclusion, consistent with our and other previous reviews, the results of the presence or lack of differences in reproductive costs between females and males are not uniform, and they are dependent on plant species, and spatial and temporal allocation patterns. Finally, we did not argue that it is meaningless to study relative reproductive costs between the sexes in plant species (Hultine et al. 2016; Juvany and Munné-Bosch 2016; Liu et al. 2021b).

Funding

This work was supported by the Natural Science Foundation of China (U1803231).

Conflict of interest statement. The authors declare that they have no conflict of interest.

Journal of Plant Ecology (JPE) was founded in 2008. It is sponsored by the Botanical Society of China and the Institute of Botany, Chinese Academy of Sciences, and published by Oxford University Press, UK. JPE publishes diverse types of articles that fall into the broad scope of plant ecology, including plant ecophysiology, population ecology, community ecology, ecosystem ecology, landscape ecology, conservation ecology, evolutionary ecology, theoretical ecology and global change ecology.

JPE has transferred to fully Open Access since July 2021, making the full text freely available for readers and authors. JPE serves as an important medium for plant ecologists worldwide to publish their research findings. Here, we present a bibliometric analysis (Aria and Cuccurullo 2017) to visualize the publication statistics and the document network of research papers published in JPE during 2017–2021.

The raw dataset was downloaded from the Web of Science Core Collection on 18 October 2022, including the fields author, title, journal title, cited frequency, abstract, address, affiliation, publication type, author keywords, keywords plus, Web of Science category, research field, references and the number of references. The raw data were manually cleaned, duplicated and items not related to research (4 editorials, 3 corrigenda, 2 commentaries and 1 data paper) removed, resulting in 472 items (466 research articles and 6 review articles) that could be further analyzed. All analyses were conducted using R v.4.2.1 (R Core Team 2022).

Publication overview of JPE

During 2017–2021, JPE published an average of 96 articles annually and had an acceptance rate of 28.2% (Table 1). From the start of JPE in 2008 up to the study period, both the number of submissions and the number of published articles tripled (Schmid et al. 2018; Zhang et al. 2020c). In addition to the traditional research and review papers, JPE has also published data papers, method papers as well as perspective and commentary papers (Fig. 1).

Figure 1:

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The annual publications in JPE during 2017–2021.

Most productive authors, countries and institutions for papers published in JPE

During 2017–2021, a total of 1890 authors published their works in JPE. The 10 most prolific authors come from three different countries and six of them obtained more than 100 citations (Table 2a). Among all articles, 229 are from institutions in China, accounting for 48.5% of the total publications in the journal. These articles received 1365 citations (Table 2b).

The authors of articles published in JPE during 2017–2021 are from 618 institutions. The top 10 institutions in terms of number of publications are shown in Table 2c. The Chinese Academy of Sciences system is the most productive institution, which includes the University of Chinese Academy Sciences, Institute of Botany, Institute of Geographic Sciences and Natural Resources Research and Institute of Applied Ecology. It is then followed by Peking University and the University of Zurich (Table 2c).

Most cited articles of JPE

The 10 most cited papers among the published papers in JPE during 2017–2021 and 2020–2021 are presented in Table 3. Among the first set, most papers were published in 2017, and two were published in 2018 (Gioria et al. 2018; Rodrigues et al. 2018) (Table 3a). In particular, the special issue on ‘Biodiversity–Ecosystem Functioning’ in 2017, including 24 research articles and 1 editorial, received high citations. Six articles from this special issue ranked among the 10 most highly cited papers from 2017–2021 (Bu et al. 2017; Huang et al. 2017; Li et al. 2017; Schmid et al. 2017; Scholten et al. 2017; Sun et al. 2017). To evaluate the performance of recently published papers in JPE, we also analyzed the 10 most highly cited articles within the past 2 years (2020–2021; Table 3b). Two articles published during this period are included in top 10 list for the entire period 2017–2021 with citation-per-year values of 7.33 (Li et al. 2020) and 6.50 (Liu et al. 2021), respectively.

Co-occurrence network of keywords

The co-occurrence network of KeyWords Plus in JPE was generated using the ‘biblioNetwork’ function in the ‘bibliometrix’ package (Aria and Cuccurullo 2017) (Fig. 2). The definition of KeyWords Plus by Web of Science is that ‘KeyWords Plus are index terms automatically generated from the titles of cited articles. KeyWords Plus terms must appear more than once in the bibliography and are ordered from multi-word phrases to single terms. KeyWords Plus augments traditional keyword or title retrieval.’ (Web of Science Core Collection Help; https://images.webofknowledge.com/images/help/WOS/hp_full_record.html). In the co-occurrence network, a total of 50 keywords are displayed based on the points’ relative position (Singh et al. 2022) and grouped into four clusters. The red zone (Cluster 1) indicates the diversity theme, the green zone (Cluster 2) represents the climate-change theme, the purple zone (Cluster 3) shows the theme of evolution and the blue zone (Cluster 4) displays the theme of plants. Briefly, diversity and climate change are the main topics that appear mostly in research articles published in JPE during 2017–2021 (Fig. 2).

Figure 2:

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Co-occurrence network of keywords plus in JPE papers during 2017–2021.

Conceptual structure map of keywords

A conceptual structure map of keywords was created based on multiple correspondences analysis (MCA). The conceptual structure map shows the relationship between one word and another by regional mapping, and each word is positioned according to the values of dimension 1 (Dim 1) and dimension 2 (Dim 2). MCA is used in bibliometric analysis, to develop a map between words with relatively similar values (Rahaman et al. 2022). The conceptual structure map can be used to identify clusters of documents that express common concepts (Aria and Cuccurullo 2017). A total of 50 words were grouped into two clusters on the map. The red zone (Cluster 1) represents the theme of climate change (how plants respond to environmental changes), and the blue zone (Cluster 2) indicates the theme of evolution (Fig. 3). In addition, the red zone includes a higher number and variety of words, suggesting that many research articles published in JPE during 2017–2021 are relevant to these themes shown in this region (Fig. 3). Moreover, the documents that make the most contribution associated with the two clusters are shown in Table 4, and five papers are detected for each of the cluster. The five articles with high contributions in Cluster 1 focused on plant communities (Ochoa-Hueso et al. 2021; Wei et al. 2019; Xu et al. 2020; Zhang et al. 2020a, 2020b), and the other five articles most representative of Cluster 2 focused on specific plant species (Kirschbaum et al. 2021; Liu et al. 2020; Smith et al. 2021; Yu and He 2021; Zeng et al. 2017).

Figure 3:

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Conceptual structure map of keywords plus in the JPE papers during 2017–2021.

Thematic analysis through bibliographic coupling

The thematic map of keywords is created with 250 words being grouped into 17 clusters. The sizes of the bubbles on the map depend on the number of publications in which the keywords appear (Rejeb et al. 2022). Themes with high density and high centrality, appearing in the first quadrant and namely motor themes, have strong internal and external ties, which are important and well developed. Themes with high density and low centrality, namely niche themes, have well-developed internal ties and marginally significant external ties, which appear in the second quadrant. Themes with low density and centrality in the third quadrant, namely emerging-or-declining themes, have both weak internal and external ties. Themes with low density and high centrality appearing in the fourth quadrant, namely basic themes, suggest well-developed external ties and unimportant internal ties. As shown in the map (Fig. 4), the themes including the keywords of rain-forest, leaf traits and leaf area are important and well developed in JPE during 2017–2021.

Figure 4:

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Thematic map of keywords plus in the JPE papers during 2017–2021.

In conclusion, as a relatively young journal dedicated to all fields of plant ecology, JPE has established distinct features covering topics from microcosm to macrocosm, with diversity and climate change as the most frequently appearing key words. We encourage authors to submit their manuscripts from widely ranging topics of classical and contemporary ecology to JPE. We thank the authors, editors and readers for their consistent support to JPE, and we continue to aim building JPE as an internationally recognized journal with global impact.

Conflict of interest statement. The authors declare that they have no conflict of interest.