1. Introduction

Plant-animal interactions are formed and maintained by signals and the transmission of energy (Schaefer et al., 2004; Sinnott-Armstrong et al., 2020; Neu et al., 2023). In mutualistic interactions, plants generally offer nutritive reward (e.g., nectar, fruit pulp, elaiosome) to attract potential pollinators or seed dispersers, and in some cases, plants signal their reward through visual or olfactory cues (Schaefer et al., 2008; Cazetta et al., 2012; Nevo et al., 2019; Stephens et al., 2020). Plants have evolved to exploit deceptive signals that attract potential pollinators or seed dispersers but provided little reward, which is common in mimicry systems (Schaefer and Ruxton, 2009; Pfeiffer et al., 2010; Midgley et al., 2015). In these mimicry systems, plant–animal interactions usually involve a tripartite of players: the mimic, the model, and the dupe (Pasteur, 1982).

Mimetic-seed dispersal involves a tripartite interaction between the mimetic seeds (the mimic), the fleshy fruits, arillate seeds or perhaps insects (the model), and frugivorous birds (the dupe). Mimetic seeds (or imitative seeds), a group of highly conspicuous seeds with little nutritive reward (e.g., fleshy aril, pulpy testa), have been proposed to mimic fleshy fruits or arillate seeds consumed by frugivorous birds (van der Pijl, 1982). They usually have a glossy appearance with contrasting red, black, or red-black seed color, smooth but hard seed coat, are retained on the mother plant for prolonged time, and contain certain toxic secondary metabolites (van der Pijl, 1982; Peres and van Roosmalen, 1996; Galetti, 2002, Tables 1 and 3). Previous research has identified at least 46 mimetic-seed species in 24 genera and 10 families, with most cases occurring within the Fabaceae, and has shown that mimetic-seed species are predominantly found in tropical regions (Table 1 and Fig. 1). Additionally, we define potential mimetic-seed species as those that produce seeds sharing similar characteristic of mimetic seeds, most of which are within the same genus as reported mimetic-seed species (Appendix A).

Four non-exclusive hypotheses have been proposed to elucidate the phenomenon of mimetic-seed dispersal: deception (mimetism or parasitism), mutualism, aposematism, and exaptation. The deception hypothesis suggests that mimetic seeds mimic fleshy fruits to attract birds for seed dispersal while providing little reward in return (van der Pijl, 1982; Galetti, 2002; Pizo et al., 2020). The mutualism hypothesis, proposed by Peres and van Roosmalen (1996), also referred to as the "hard-seed for grit" hypothesis, posits that mimetic-seed dispersal is mutually beneficial for both birds and mimetic seeds. For birds, especially those terrestrial omnivorous birds, the hard mimetic seed may function as mineral grit to enhance digestive efficiency. For mimetic seeds, the digestive process in the bird gut breaks seed dormancy without causing damage, resulting in a higher seedling germination rate. The aposematism hypothesis suggests that the red seeds (e.g., seeds of Ormosia species) may act as a deterrent to seed predators by signaling the presence of toxic alkaloids, thus serving as an aposematic cue (Foster and Delay, 1998). The exaptation hypothesis argues that conspicuous color of mimetic seeds sharing similar seed coat characteristics with non-mimetic-seed species (e.g., plant species within the same genera) but not dispersed by birds could be considered exaptation (Galetti, 2002). The exaptation hypothesis also suggests that dormancy protects mimetic seeds against deterioration before dispersal (Brancalion et al., 2010). Although each hypothesis has been supported by some evidence, support remains controversial due to experimental conditions. In addition, relatively little research has been done on the ecological functions of the visual, olfactory, gustatory, and tactile signals displayed by mimetic seeds, as well as their independent or coupled effects.

In this mini-review, we use information of reported and potential mimetic-seed species throughout the world to discuss key characteristics of mimetic seeds. We focus on three questions: 1) How did the current geographical distribution of mimetic-seed species form? 2) Why do mimetic seeds usually have high conspicuousness but provide little nutritive reward for frugivorous birds? 3) What is the ecological and evolutionary significance of key characteristics of mimetic seeds and their secondary metabolites? Further, we propose approaches to study the evolutionary ecology of mimetic-seed dispersal.

2. The global distribution of mimetic-seed species

Preliminarily analysis of the global distribution of mimetic-seed species was done in R (R Core Team, 2023). We first downloaded raw occurrence data of mimetic-seed species from GBIF database using package "rgbif" (Chamberlain et al., 2024), then cleaned the data using package "CoordinateCleaner" (Zizka et al., 2019) to remove outliers (e.g., occurrence data located at sea). After that, we uploaded the cleaned data on the interface of the package "wallace" (Kass et al., 2023) to thin data (the "Thinning Distance" was set as 100 km, ca. 1° latitude apart) and thus presented data more clearly without changing the distribution pattern of mimetic-seed species. We visualized the thinned data using package "maps" (Becker et al., 2023) and "ggplot2" (Wickham, 2016).

We found that mimetic-seed species occur in both tropical and temperate regions, but mainly in the tropics (ca. 74%, Fig. 1a; Appendix A). Species density peaks near the equator and decreases with increasing latitude north and south (Fig. 1c), nearly consistent with global patterns of bird richness (Gaston, 2000). Previous studies have demonstrated the ubiquitous interspecific and intraspecific competition among fruiting species for bird dispersers in the tropics (Howe and Estabrook, 1977; Manasse and Howe, 1983; Poulin et al., 1999). Fedorov (1966) has reckoned that in the absence of interference in the tropics, competition mainly occurs between species sharing similar ecological niches. He also believed that the origin of phylogenetic species may be caused by a few mutations that subsequently directly or indirectly alter the morphogenesis of different species. We thus hypothesize that one possible explanation for the occurrence of mimetic-seed species is gene mutation in phylogenetically related non-mimetic-seed species under the selection by bird dispersers in the tropics.

Mimetic-seed species density was found to be high along coastal areas and on small islands (Fig. 1a). One reason for such a distribution could be seed dispersal by ocean current, as has been documented in Abrus precatorius (Murray, 1986) and Ormosia monosperma (Torke et al., 2022). However, birds may also provide trans-oceanic seed dispersal (Nogales et al., 2012).

3. Interaction between mimetic seeds and their bird dispersers

Mimetic-seed dispersal has been reported in several studies (Table 2). During seed dispersal interactions, birds can select fruit traits using their outstanding visual capability, as well as relatively poorer tactile, gustatory, and olfactory capabilities (Ridley, 1930; van der Pijl, 1982; Willson and Whelan, 1990; Corlett, 2011; Renoult et al., 2013). Birds also learn to associate pre-ingestive sensory cues with post-ingestive feedback to acquire foraging experience (Schaefer et al., 2008; Corlett, 2011). Notably, seed traits can interact with the digestive processes of bird dispersers, and subsequently influence seed fate (Kleyheeg et al., 2018). Thus, we hypothesize that the characteristics of mimetic seeds interact with the sensory capabilities and the digestive strategies of the different bird dispersers.

Mimetic seeds have been shown to attract birds using conspicuous visual cues. Many birds have cone visual pigments that are ultraviolet-wavelength sensitive (UVS) and long-wavelength sensitive (LWS) (Hart, 2001). Thus, birds can quickly detect conspicuous fruits with high reflectance at long wavelength and/or ultraviolet wavelengths, such as red fleshy fruits and berries with waxy bloom (Burkhardt, 1982; Schaefer et al., 2006). Moreover, smooth and waxy testa of mimetic seeds of several species, such as Erythrina caffra (Fig. 2a) and Abrus precatorius (Fig. 2c), likely amplify the conspicuousness of seeds to bird dispersers by reflecting ultraviolet light. In addition, fruits with contrasting colors are also conspicuous to avian vision (Schmidt et al., 2004; Melo et al., 2011). Studies have shown that red fruits have higher chromatic contrast, whereas black fruits have higher achromatic contrast against the same background (Schaefer et al., 2006). These red-black bicolor fruits have also been shown to enhance fruit removal rates (Willson and Melampy, 1983). Our analysis indicates that most mimetic seeds are red and/or black (Table 1 and Fig. 2), which is consistent with the idea that mimetic seeds can further increase conspicuousness by maximizing color contrast against the same background.

Mimetic seeds may deceive birds into seed dispersal through food resource mimicry. The main colors of bird-dispersed fleshy fruits are red and black (Willson and Whelan, 1990; Schaefer and Schaefer, 2007), indicating a potential convergence among fleshy-fruited species. Birds have been shown to associate fruit colors with nutritive reward (Schaefer et al., 2008). Some birds, however, may be subject to "receiver bias" (Schiestl, 2017) and may be disproportionately drawn to conspicuous red or black colors during their foraging process. For example, naive birds of some species tend to prefer red and/or black fruit (Schmidt and Schaefer, 2004; Duan et al., 2014). Burns (2005) found that, compared with orange fruits, the red fruits of Rubus spectabilis attracted more birds by mimicking the sympatric red fruits of R. parviflorus, implying that the red signal could be vital for the occurrence of mimicry between the mimic and their sympatric model. Another distinct group of mimetic seeds (e.g., seeds of Margaritaria nobilis, Pollia condensata and Rhynchosia mannii) display bluish colors (van der Pijl, 1982; Cazetta et al., 2008; Vignolini et al., 2012, Fig. 2e). Interestingly, such bizarre bluish colors are assumed to mimic the appearance of insect prey to deceive insectivorous birds or to attract birds for nest decoration or mating (van der Pijl, 1982; Vignolini et al., 2012). Thus, mimetic seeds may deceive birds by mimicking the appearance of their food or other resources, probably with sympatrically occurring fleshy fruits being mimicked at high frequency.

We examined color similarity between mimetic seeds and fleshy fruits by measuring reflectance data of several mimetic seeds and fleshy fruits. We then constructed a tetrahedron color space for UVS-birds using the R package "pavo", in which color was presented as a point (Goldsmith, 1990; Maia et al., 2019). We found that UVS-birds may not be able to distinguish several mimetic seeds from fleshy fruits (Fig. 2j and k). We thus assume that the red and/or black colors of mimetic seeds are an adaptation to the color vision of bird dispersers. Galetti (2002), however, has argued that the color of mimetic seeds is an exaptation rather than adaptation to present-day bird dispersers, noting the color of mimetic seeds may result from phylogenetic constraints. These two conjectures require further research.

Deceptive mimetic-seed dispersal is affected by three main factors: the foraging experience and learning ability of different birds, environmental heterogeneity, and the density of mimetic-seed species. Mimetic seeds can sporadically deceive birds to dispersal, especially those naïve individuals lacking foraging experience, as in seed dispersal of Ormosia arborea and Rhynchosia melanocarpa (Galetti, 2002; Pizo et al., 2020). It is assumed that as birds increase their foraging experience, the efficiency of mimetic-seed dispersal will decrease. Mimetic-seed species seem to adopt different fruiting tactics in heterogenous and homogenous environments. For example, in more homogenous forests in south-east Brazil, Ormosia arborea produce dehiscent pods with mimetic seeds for long time, thus, benefitting from remaining relatively rare in the community all year, producing an even dispersal pattern (Galetti, 2002). In a heterogenous environment, Rhynchosia melanocarpa is thought to benefit more from the "willingness" of birds to eat fruits and potential migratory bird dispersers by producing mimetic seeds relatively abundant early in the fruiting season (Pizo et al., 2020). In addition, environmental heterogeneity can disrupt foraging memory and lower the foraging efficiency of birds (Hirvonen et al., 1999), which may increase mimetic-seed dispersal by birds. The density of mimetic-seed species is generally low (Peres and van Roosmalen, 1996; Foster and Delay, 1998; Pizo et al., 2020). If it increases in the environment, this will inevitably influence the fitness of bird dispersers, because they have fewer eatable food sources. As a response, some birds will seek food in other places, which, will decrease the dispersal frequency of mimetic seeds in turn.

Mimetic seeds often remain intact through the digestive system of bird dispersers because of their smooth and hard exterior. The smoothness of mimetic seeds may enhance the ingestion rate by avian species, thereby leading to a delayed ingestive response. This delay could potentially hinder the development of foraging experience in birds, ultimately promoting the dispersal of mimetic seeds. Yet there is a possible trade-off: smooth mimetic seeds that benefit from rapid dispersal suffer from short dispersal distances. For example, mimetic seeds of Erythrina caffra are too smooth for birds to take easily, causing many seeds to fall into the seed shadow of the mother plant (G. Chen, personal observation). According to the "hard-seed for grit" hypothesis, the hardness of mimetic seeds serves as a crucial factor in facilitating the mutualism between mimetic seeds and bird dispersers. This is attributed to its ability to enhance digestion by birds and mitigate seed damage resulting from avian digestion. Furthermore, seed hardness has the potential to increase seed survival rates following consumption by grazing animals, reduce predation by rodents, prevent deterioration during the rainy season prior to dispersal, regulate germination timing, and contribute to the establishment of a resilient soil seed bank (Taylor, 2005; Brancalion et al., 2010; Paulsen et al., 2013). However, the foraging habits (for example, frugivory, herbivory or insectivory) and the foraging maneuvers (for example, perch-plucks, sally-plucks or hover-plucks) employed by birds will directly affect their digestive capabilities, and therefore influence the seed fate of any mimetic seeds eaten. Terrestrial granivorous birds have more powerful digestive guts and are able to abrade the hard coats of mimetic seeds, thus benefiting the germination of excreted seeds (Peres and van Roosmalen, 1996; Foster and Delay, 1998). Compared to terrestrial birds, arboreal bird dispersers can carry mimetic seeds farther from the mother plant, particularly during periods of fruit scarcity (Foster and Delay, 1998). However, the impact of such variation on seed fate in mimetic-seed dispersal remains unclear, as digestive capability varies among bird species (Gionfriddo and Best, 1996; Rehm et al., 2019).

4. The potential function of key secondary metabolites in mimetic seeds

Mimetic-seed species have allocated energy to certain secondary metabolites to form key functional characteristics, including conspicuous color, hard seed coat, certain toxic secondary metabolites, and perhaps a smooth waxy layer. The spatiotemporal variation of those characteristics may primarily be based on the evolution of certain key secondary metabolites. Red or black pigments may result from the presence of anthocyanins, carotenoids, or perhaps alkaloids (Lancaster et al., 1997; Schaefer et al., 2008; Roy et al., 2022), and the bluish structural colors of several mimetic seeds largely originate from the helical cellulose (Vignolini et al., 2012, 2016). Hardness may depend on the presence of phenolic compounds (Mohamed-Yasseen et al., 1994). The evolution of the waxy layer may have occurred together with that of the metabolism of long-chain fatty acids (Place and Stiles, 1992; Kunst and Samuels, 2009). Mimetic seed toxicity may result from certain toxic secondary metabolites, especially alkaloids.

Although relatively rare, alkaloids are found in mimetic seeds of several species, such as Abrus precatorius. Some alkaloids may be detrimental to rodents, birds and perhaps also to humans (Table 3). For example, quinolizidine alkaloids in the seeds of Ormosia arborea can inhibit seed predation by agoutis (Guimarães et al., 2003). Notably, Foster and Delay (1998) proposed that seed predators may be deterred by the aposematic red seed color of Ormosia species, since it might signal the presence of toxic alkaloids. Although this hypothesis has been refuted in subsequent research (Galetti, 2002), it is reasonable, as the presence of functional alkaloids in different plant tissues (roots, flowers, etc.) are associated with the bright red signal (He et al., 2017; Roy et al., 2022). If it is true, there would exist a possible trade-off behind the bright red signal of mimetic seeds, attracting birds on the one hand, but causing them damage on the other. Several toxic alkaloids, however, may not be harmful to birds (Cipollini and Levey, 1997).

The specific secondary metabolites contributing to those key characteristics in mimetic seeds, however, remain largely unknown due to a lack of research or limited analytical techniques. Our field observation showed that Pittosporum tobira, a potential mimetic-seed species, deceived birds into dispersal by its bright reddish seed color. The seeds of P. tobira have been reported to contain novel pittosporumxanthins A1 and A2, suggesting the red seed color is attributed to highly stable C₆₉ carotenoids (Fujiwara and Maoka, 2001). Intriguingly, during our behavioral experiments, the reddish seed color of P. tobira remained nearly unchanged even after passing through the guts of the frugivorous bird Pycnonotus xanthorrhous, further indicating that it could be a deceptive signal (Fig. 2f, g, h and i). The reddish seeds of E. caffra also deceives birds into dispersal. However, the main pigment of its reddish signal remains as yet unidentified, probably due to its low detection limit and unique characteristics (Fig. 2b). Evaluating the evolution of key secondary metabolites in mimetic seeds is thus challenging but meaningful.

5. Future directions

Evolutionary games usually consist of different players, payoffs, and strategies, accompanied by the variation of continuous traits of different players (Riechert and Hammerstein, 1983; McGill and Brown, 2007). We consider mimetic-seed dispersal an evolutionary game between mimetic-seed species, fleshy-fruited species, and their bird dispersers. The respective fitness of each player is the payoff of the game, and each player evolves optimal strategies to gain fitness. We assume that mimetic-seed species have adopted an "energy-reallocation strategy" (i.e., mimetic-seed species allocate energy to produce key secondary metabolites rather than to form nutritive seed tissues which could benefit birds), while fleshy-fruited species have adopted a "reward strategy" (i.e., providing a nutritive reward to birds) to attract birds for seed dispersal. In the "energy-reallocation strategy", if allocating energy in key secondary metabolites can suppress the cost of producing nutritive reward, it would be more profitable for plant fitness. It is expected that a portion of sympatric species currently with fleshy fruits may eventually evolve an "energy-reallocation strategy". However, if the true metabolizable energy (TME) provided by mimetic seeds for birds is lower than that provided by fleshy fruits, the fitness of birds would decrease. Once the frequency of mimetic-seed species increases in the environment, this will inevitably influence the fitness of bird dispersers. Consequently, some birds may seek food resources with higher TME value elsewhere, subsequently reducing the fitness of both mimetic seeds and fleshy fruits. Untangling this dynamic game can therefore shed light on the ecological and evolutionary processes occurring in mimetic-seed dispersal.

There are few issues of concern. The global richness of mimetic-seed species has likely been underestimated (Appendix A). In addition, little is known about the evolution of several key characteristics or the evolution of secondary metabolites related to them. In this mini-review, we have discussed four hypotheses that attempt to explain mimetic-seed dispersal. Our preliminary work supports the parasitism (deception) hypothesis, however, further research should continue to test the remaining hypotheses.

Here, we propose five approaches to study mimetic-seed dispersal in the future. 1) Seed dispersal mode (i.e., by ocean current or birds) should be classified for mimetic-seed species (including potential mimetic-seed species) growing along coastal areas and sympatric fleshy-fruited species. 2) We should also integrate occurrence data of mimetic-seed species with global climate data, allowing predictions on distribution pattern of global mimetic seeds in the future. 3) The key characteristics of mimetic-seed species, phylogenetically-related species, and sympatric fleshy-fruited species should be evaluated. Specifically, future research should evaluate dispersal mode, seed color, seed hardness and seed nutriment of these plant species. This evaluation of characteristics should include estimations of divergence times and reconstructions of ancestor characters and ancestor range. 4) Future studies should identify the structures of specific secondary metabolites related to key characteristics of mimetic seeds. One potentially rewarding approach would be to use multi-omics to analyze their spatiotemporal variation. 5) We also recommend using ''game theory" to decode interactions between mimetic-seed species, fleshy-fruited species, and their bird dispersers, especially calculating the true metabolizable energy value of mimetic seeds and their sympatric fleshy fruits for bird dispersers.

Acknowledgements

We thank Dr. Eliana Cazetta for providing the raw photo of Fig. 2e, Dr. Zhe Chen for analyzing spectral reflectance data (Fig. 2j and k) and giving some helpful comments on the manuscript, Zhi Chen for providing the raw photo of Fig. 2d, Zhi Chen and Zai-Qiu Xiong for performing behavioral experiments, Dr. Alison Jane Marczewski and Dr. Jia Ge for conducting some scientific correction. This work was supported by the Yunnan Ten Thousand Talents Plan Young & Elite Talents Project (YNWR-QNBJ-2018-017), the National Natural Science Foundation of China (32371564) and the Key Project of Basic Research of Yunnan Province, China (202101AS070035; 202301AS070001) to G. Chen, and Yunnan Provincial Science and Technology Talent and Platform Plan (202305AM070005).

CRediT authorship contribution statement

Min-Fei Jin: Investigation, Data curation, Formal analysis, Writing original draft, Writing − review & editing, Visualization. Xiang-Hai Cai: Methodology, Resources, Validation. Gao Chen: Conceptualization, Writing − review & editing, Supervision, Funding acquisition.

Declaration of competing interest

No potential conflict of interest was reported by the authors.

Appendix A. Supplementary data

Supplementary data to this article can be found online at https://doi.org/10.1016/j.pld.2024.07.006.