1. Introduction

In the natural environment, plant reproduction via seed faces many challenges. Firstly, the seeds need to be dispersed from the parent plants to reduce density-related mortality (Wright et al., 2016; Wandrag et al., 2017; Landim et al., 2022). Over 75% of tree species in the tropics and 30–40% of plant species in temperate regions depend on animals for fruit and seed dispersal, whilst the remaining species have diaspores dispersed by wind and water, or by explosive dehiscence of the fruits (Valenta et al., 2015; Jordano, 2016; Neuschulz et al., 2016; Lee et al., 2022). Secondly, seeds must germinate at a time that ensures subsequent seedling establishment, so that population recruitment is successful (Caughlin et al., 2016; Dias et al., 2024).

As many fruits and seeds are an integral component of the diet of animals, they can be consumed or partly destroyed while being disseminated to new sites (Janzen, 1969, 1971; Pérez-Camacho et al., 2023; Santos et al., 2023). Specific patterns of animal behaviour in handling fruits can significantly affect the survival and germination of seeds (Fig. 1). Generally, frugivorous bats, marsh birds and some terrestrial mammals, especially primates, consume the fruits but leave the relatively large seeds unharmed (Seltzer et al., 2015; Sánchez and Dos Santos, 2015; Bregman et al., 2016; Nowak et al., 2019). These seeds contribute to essential population (re)distribution when deposited at sufficient distances from parent trees and when conditions are appropriate for germination and seedling development in the natural ecosystem (Jaroszewicz et al., 2023). By adopting a rather similar mechanism, myrmecochorous plants produce seeds with a lipid-rich appendage, the elaiosome, to attract ants for dispersal (Calvino-Cancela and Rubido-Bará, 2012; Hilley and Thiet, 2015). Ants take the seeds to their nests, and after larvae have consumed the elaiosome, intact seeds germinate with little hindrance.

Other invertebrates and vertebrates can cause substantial physical injuries to seeds or even exert total seed loss during consumption of fruits at pre- and post-dispersal, unless the seeds are well protected morphologically and physiologically (Robertson et al., 1990; Gardener et al., 1993; Naranjo et al., 2003; Bravo, 2008; Mancilla-Leytón et al., 2012; Zeng et al., 2022; Rehling et al., 2024). Seeds may suffer more severe damage if handled more than once by different animals, depending on the seed attributes, and the abundance of frugivores and granivores driven by micro-habitats favorable for the multiple predators. Seeds with defects left in contact with soil are also susceptible to infestation by soil microorganisms. Depending on the degree of injuries and secondary microbial infestation, the damaged seeds can have declined vigour and reduced resources for the development of seedlings. Simultaneously, many abiotic stressors, being parallel or additive, ultimately reduce the regeneration capacity of the plant species significantly, threatening the ecological structure.

Considering the need to harness the services of foraging animals to enable growth in new environments, reciprocal pressures on seeds and granivores have driven adaptations and the development of mutualisms rather than antagonisms (Mezquida and Benkman, 2014; Arieira et al., 2016; Mori et al., 2018; Dou et al., 2024). The community richness and the concurrent control of seed predators within natural sites generally regulate the seed predation intensity and protect the integrity of plant regeneration from seeds. Moreover, some seeds can endure the loss of a certain level of biomass and parts to counter predation stresses and retain the capability to germinate and produce healthy seedlings post-predation (Fig. 1). Field studies have revealed the possible ecological contributions of damaged seeds for ecosystem stability (Perea et al., 2018; Palmer and Catterall, 2021). Meta-studies in laboratories and greenhouses have also shown successful sprouting and plantlet development despite simulated incision and clipping of seeds (McEuen and Steele, 2005; Leiva et al., 2018). However, the ability of damaged seeds to germinate following predation is species-specific. Orthodox (desiccation tolerant) seeds and recalcitrant (desiccation sensitive) seeds can have different strategies in facing handling by their dispersing animals. For example, orthodox seeds with physical dormancy are always protected by thick coverings, enabling them to even survive ingestion and defecation by their predators (Oliveira et al., 2023; Trabelsi et al., 2023). There are also recalcitrant seeds enclosed in a hard endocarp, making them rather resistant to damage. Other orthodox and recalcitrant seeds tolerate a certain degree of reserve loss during animal dispersal, thus ensuring ecological stability.

Within the past few decades, researchers have reported the germinability of seeds with physical defects caused by hoarding animals in relation to inadvertent and effective seed dispersal. While many factors affect the survival of seeds following predation, the desiccation sensitivity of seeds and any associated morphological and physiological features may have also shaped certain patterns of seed-animal relationships in ensuring species' natural ecological fitness. This aspect of seed ecology has been less examined. This review consolidates current knowledge of seed-predator co-existence and adaptations in both orthodox and recalcitrant seeds that ensure reproduction success despite physical injuries. We also elucidate the sprouting potential from cotyledonary fractions exclusively demonstrated by recalcitrant seeds of certain families. For the newly formed seedlings at post-predation, we briefly discuss the impact of subsequent herbivory and environmental conditions on seedling performance. Lastly, we suggest some possible future work to correlate seed-granivore adaptations and to reveal greater understanding of the persistence of seeds with different physical defects. Such adaptive seed traits enable species to thrive and maintain the habitat's functional plant composition and sustain overall ecological stability.

2. Defence strategy

Survival of physically damaged seeds is often related to the type and magnitude of injuries (Fig. 1). According to the optimal defence theory, the vital parts in seeds must be protected against the ravages of predators (Pavia et al., 2002; Rehling et al., 2024). This theory has also been applied to plant vegetative tissues. In principle, plants allocate more energy to protect essential tissues which, if damaged or lost, can be associated with significant declines in plant performance, or even mortality. To accomplish reproduction in the natural environment, a seed should contain an intact embryonic axis attached to (i.e., cotyledonous, non-endospermic) or have access to (endospermic) nutrient reserves to complete germination. Thus, seeds which depend on animals for effective dispersal are equipped with unique morphological and physiological adaptations to resist or tolerate potentially catastrophic biotic stresses (Applegate et al., 1979; Althoff et al., 2004; Tjelele et al., 2012; Perea et al., 2018).

2.1. Covering effect

To avoid faunal consumption, some seeds invest significant resources in the development of hard coats (testa or endocarp) as a physical barrier to protect the embryo (Fig. 1 and Table 1). By virtue of the lignified coverings, large seeds regurgitated or spat out by the animals after consumption of the fruit pulp are mostly intact. As hard seeds often have physical dormancy, as a bet-hedging strategy against unguaranteed conditions for seed germination and seedling establishment, they can form soil seed banks (Baskin and Baskin, 2004; Lan et al., 2018; Wu et al., 2024). Scarification of the seed coat by soil chemicals and microbial reactions, and exposure to other environmental factors, including large temperature fluctuations, can breach the coat and render the seed permeable to water and permit germination (Ofori et al., 2015; Sone et al., 2016; Hu et al., 2018; Wu et al., 2024). Examples of seeds that depend on their coat to reduce injuries during dispersal and predation by animals extend to at least 30 families and 41 genera (Table 1). Seeds equipped with thick covering are mostly orthodox seeds. In the case of small orthodox seeds having hard coats within fruits, the whole seeds may survive consumption and even benefit from animal ingestion in terms of modified seed-coat traits through chemical (acid) scarification (Fig. 1). Thus, physical dormancy in the seeds is overcome when the coat is abraded and becomes permeable to water (and gases) after passing through the predators' digestive tracts and the seeds can achieve earlier and higher germination, demonstrating mutualism to thrive in natural environments (Trabelsi et al., 2023; Awasthi et al., 2024). Conversely, recalcitrant seeds with thin coverings mostly do not survive mastication and the enzymatic reactions associated with ingestion and excretion (Weiss et al., 2022).

In a different survival strategy, some desiccation sensitive seeds with papery seed coats, for example those of Calatola laevigata (Metteniusaceae) and Canarium odontophyllum (Burseraceae) from the tropical rainforests, are shielded by lignified and thick endocarps (Table 1). These recalcitrant seeds with fleshy embryos of 20–40 mm in size and copious endosperm are highly vulnerable to physical injury (Vallejo-Marín et al., 2006; Masarip et al., 2020). Often, complete fatality follows a very low level of injury mainly because of the susceptibility of the damaged seed tissues to secondary fungal and pathogen attack. For the same reason, many recalcitrant seeds in the Arecaceae are also protected by their hard endocarp, but such a covering of these desiccation sensitive seeds allows water uptake when left at moist sites after the terrestrial mammals have consumed the juicy fruit pulp (Table 1; de Barros Leite et al., 2012). Then, the seeds germinate and access water from the soil, and the primary shoots soon gain photosynthetic capability.

Without resistant coats that cover the entire seeds, the geometry of seeds presents a natural mechanism of predation avoidance or reduction. A seed can have a much thicker protective layer encasing the radicle-hypocotyl axis, whilst other parts have thinner coverings to be 'sacrificed' to granivores. With thicker pericarp at the apical ends, acorns of many recalcitrant Quercus spp. protect their regenerative tissues from weevil and moth attacks (Yi and Yang, 2010; Sone et al., 2016). Thus, adult females oviposit at the basal sides of the acorns. These insects usually complete their juvenile development within the large acorns without reaching the vulnerable areas containing the embryonic axes. Thus, the high level of recurrent larval attack generally does not impede acorn germination.

2.2. Embedded embryo

Another morphological adaptation to reduce the risk of injury is to embed the embryo or embryonic axis further into the seed rather than locating these plant-to-be tissues at the apical or basal ends (Fig. 1). For example, in Quercus mongolica (Fagaceae; recalcitrant) and Pittosporopsis kerrii (Icacinaceae; desiccation tolerance to be confirmed) seeds, the embryonic axes are located deeper within large cotyledons and avoid nibbling damage by small mammals, such as squirrels and rodents (Cao et al., 2011; Zhang et al., 2014; Yi et al., 2015). For Q. mongolica, the embryonic axis is buried 0.76 cm deep in the cotyledon, and the removal of 4 mm of cotyledon at the apical end does not impact germination, which is not the case for some other acorn species - Quercus variabilis, Q. acutissima, Q. aliena and Q. serrata (Zhang et al., 2014). Embedding the axis this deep in the acorn also affords some protection against cold temperature for Q. mongolica in its natural habitat (Chen et al., 2025). As ovule shape and the orientation of the zygote during embryogenesis underlie the polarity of a seed, other highly complex physical and physiological interactions within the seed, as well as environmental cues, influence seed development. Much remains to be discovered in this branch of plant and seed ecology.

2.3. Defensive compounds

In addition to structural modifications that protect the embryos, seeds may also invest in chemical defence by synthesising compounds that directly or indirectly reduce herbivory (Fig. 1; Whitehead et al., 2013; Kozuharova et al., 2023; Zhang et al., 2024). For many highly nutritious desiccation sensitive acorns, the apical end contains much higher concentration of tannin, making this area containing the embryonic axes unpalatable to larvae (Weckerly et al., 1989; Steele et al., 1993). However, larvae may consume the apical seed part, as well as the embryonic axis, to complete their life cycle in the much smaller acorns, resulting in regeneration failure of these acorns.

Other compounds in seeds that have been reported to play a role against herbivory include phenolics, for example coumarins, alkaloids, terpenes, glucosinolates in seeds of Brassicaceae (orthodox) and sulfur-containing compounds (Nelson and Whitehead, 2021; Anjali et al., 2023; Shiade et al., 2024). These metabolites affect insect appetite, discouraging pest attack differently, while some of these compounds control secondary pathogenic infection following the unintentional opening of the seed coat and physical injuries to the seed (Andersson, 1992; Liu et al., 2012; Anjali et al., 2023). The biological activities of the compounds can also be achieved through the activation of the immunity-related genes and signaling pathways in some seeds, for example, the salicylic acid-dependent pathway (Zaynab et al., 2024).

3. Mass loss tolerance

For plants with seeds that lack defence strategies, tolerance to loss of some reserves is the other option to ensure reproduction success (Fig. 1 and Table 2). Recalcitrant seeds are generally larger than orthodox seeds (Daws et al., 2005; Subbiah et al., 2019; Dias et al., 2024). Larger recalcitrant seeds from the families Acanthaceae, Chrysobalanaceae, Clusiaceae, Fabaceae, Fagaceae, Lauraceae, Lecythidaceae, Meliaceae, Myrtaceae, Rhizophoraceae with more reserves in the cotyledons can tolerate the removal of a certain degree of seed mass by granivores without exhausting the energy and reserves required for germination (Table 2). With variations across the flowering plant kingdom, there are also yet to be discovered large orthodox seeds with abilities to withstand animal gnawing (Table 2). Larger seeds containing higher nutrition could have evolved to endure mass loss since they are more lucrative for the animals, especially for the large mammals having appropriate gape sizes, although the animal-to-seed size relationships remain controversial (Loayza et al., 2015; Ruggera et al., 2021; Villar et al., 2022; García-Hernández et al., 2023). However, other factors such as handling difficulty before consumption and storability of seeds also affect the animals' selection choices (Forget, 1992a, 1992b; Xiao et al., 2013; McConkey et al., 2015; Villar et al., 2022). On the other hand, small recalcitrant seeds measuring less than 5 mm from the family Myrtaceae can germinate after a loss of more than half of their reserves while small orthodox seeds of Lotus corniculatus also tolerate insect predation well (Ollerton and Lack, 1996; Teixeira and Barbedo, 2012; Amadar and Barbedo, 2015; Tsan, 2023). The seed size to mass loss tolerance relationships are affected by several factors, including the cellular physiology within seeds, which need comprehensive studies, especially those concerning the contributions of such seed traits to population growth in forests.

3.1. Reserve effect hypothesis

According to the reserve effect hypothesis, seed size is positively associated with the investment of energy in favour of germination. This size-related trait is also associated with superior seedling establishment despite physical defects following predation (Dalling and Harms, 1999; Landim et al., 2022; Zhao et al., 2024; Chen et al., 2025). Some large seeds are presumed oversized for germination, and thus, the large cotyledons are more important for manipulating the biotic dispersers than providing energy for the growth of the seedlings (Giertych and Suszka, 2011; Zhang et al., 2014; Leiva et al., 2018; Luo et al., 2023). The reserves are otherwise used for the maintenance of respiration to sustain slow seedling growth under low light conditions, and surplus reserves are then lost through decay.

Numerous systematic field censuses and simulated seed fragmentation studies in laboratories and greenhouses have proved that partial loss of the reserve for the energy-rich large seeds is generally sublethal, as summarised for 16 families (Table 2). In contrast, heavy predation of smaller seeds, often involving consumption of the embryos, hinders germination (Hou et al., 2010; Tella et al., 2016; Rehling et al., 2024). However, there can be substantial quantitative and qualitative variations in the mechanisms to cope with seed gnawing among large seeds. For example, large seeds of Prioria copaifera (Fabaceae; recalcitrant), Virola surinamensis (Myristicaceae; intermediate) and Gustavia superba (Lecythidaceae; recalcitrant) retain germination in the field when animals have consumed up to 60% of their cotyledons (Howe and Richter, 1982; Sork, 1987; Dalling et al., 1997; Dalling and Harms, 1999). The remaining seed fragments behave like smaller seeds, achieving normal germination post-predation, especially when the growing points (i.e., root and shoot of the embryonic axis) are not destroyed (Fig. 1). On the other hand, seeds of Damburneya ambigens (Lauraceae; recalcitrant), Couepia polyandra (Chrysobalanaceae; desiccation tolerance unknown), Licaria velutina (Lauraceae; desiccation tolerance unknown), and Dussia mexicana (Fabaceae; desiccation tolerance unknown) with similar seed sizes (or mass) tolerate removal of only up to 10% of the endosperm (Vallejo-Marín et al., 2006). They die with more loss of biomass. The downstream cellular and biochemical responses after damage are among the study aspects yet to be explored to understand why these seeds are so vulnerable to injuries.

For many legumes, their seed predators, for example the bruchinae insects, also prefer larger pods and seeds for oviposition implying the importance of seed quality for the growth and development of their juveniles. The amount of reserves lost to beetles is critical in determining the germinability of the seeds while holes made by the insect pests on the seed coat could favour germination through facilitated water and oxygen uptake (Fox et al., 2012; Sanabria-Silva et al., 2017; Talonia et al., 2022; Dlamini et al., 2024). Mortality often follows intense larval consumption of seeds as the pests also destroy the embryonic tissues. Otherwise, surviving seeds after variable predation rates could develop seedlings with slower growth rates. However, the arthropod association with the legumes also recruits other beetles that act as parasitoids and destroy the eggs and larvae of the seed-feeding pests, ensuring negligible impact on seedling recruitment (Sharratt and Olckers, 2019; Cuny et al., 2022; Oliveira et al., 2023). While past studies concluded subtle regulation of the seed predators by their parasitoids, the parasitism between the seed predators and their parasitoids is another ecological interesting subject to be explored with regards to seed resources and the spread of legume species.

3.2. Obliged dependency in mass loss tolerance

While some seed-predator relationships are not species-specific, investment into high amounts of seed biomass can be irrelevant in some plant-animal co-existence where there is an imperative requirement for some small seeds to host their specialist predators for reproduction success. Some lepidopterans, especially moths, hold dual roles of obligate pollinators and predators in their different growth stages, which influence the population resilience of both the plants and insects. A remarkable example is the co-speciation between Yucca spp. and Hesperoyucca spp. from the Agavaceae family and the moths of Tegeticula yuccasella and Parategeticula spp. (Pellmyr, 2003; Althoff et al., 2004; Song et al., 2020). The adult moths pollinate the flowers of these plants whilst their larvae feed on the small seeds, mostly orthodox in nature. Nevertheless, the larval development within the seeds does not hamper the seed germinability (Table 2). This reproduction accomplishment of both the plant and the moth represents an example of association with balanced costs and benefits. However, there are also cheater Tegeticula spp., for example Tegeticula intermedia and Tegeticula cassandra, that reap the benefit of feeding on these seeds but lack the mouthpart that can provide pollination services in return, although the larvae do not impinge the reproductive output of the plants (Segraves et al., 2005).

4. Endozoochory

In contrast to the partial loss of seed mass, endozoochory is the ingestion of the fruits with seeds in them by animals and excretion of the seeds some distances away from the parent plant (Lee and Lee, 2020; Nelson and Whitehead, 2021; Lee et al., 2022). There are many examples of seed travel through the digestive tracts of predators. Gulper type birds, bats and terrestrial megafauna such as elephants, ungulates, for example, tapirs and wild boars, and primates having appropriate gape width consume whole fruits and the small seeds within (Beavon and Kelly, 2015; Niederhauser and Matlack, 2015; Nakabayashi et al., 2016; Ohkawara et al., 2023; Lepková and Mašková, 2024). In aquatic habitats, fish and waterfowl are important fruit and seed consumers (Agami and Waisel, 1986, 1988; Weiss et al., 2022). In the floodplain forests, for example, those in the Amazon Basin, approximately 200 species of fish have a seasonal shift in diet to dropped fruits and seeds that float on the water surface during the flood period, performing pivotal roles in seed dispersal and maintenance of community dynamics (Correa et al., 2016; Kricher, 2017). Unlike host-specific insect predators, these vertebrates are mostly generalists and the types and amounts of fruits and seeds they consume are highly variable (Lee and Lee, 2020; Navarro-Ramos et al., 2024).

Several factors account for the survival of seeds following endozoochory. The digestive physiologies of terrestrial animals and avians affect the retention time and seed integrity following passage through their digestive systems (Janzen, 1982; de Barros Leite et al., 2012; Nelson and Whitehead, 2021). Some secondary metabolites in fruits may regulate gut passage of fruits and seeds thereby influencing enzymatic reaction time on seeds within the animals (Baldwin and Whitehead, 2015; Lee et al., 2022; Awasthi et al., 2024). Ultimately, seed coat modifications in the digestive tracts of animals influence the germinability of defecated seeds (Table 1). Germination only occurs when seeds are excreted unchanged, or if they remain physiologically unharmed after mechanical or chemical alteration (Jaroszewicz et al., 2023). Animal ingestion generally expedites germination of 'hard' seeds (generally not a feature of recalcitrant seeds except for some palms and Lauraceae (Jaganathan et al., 2019, Visscher et al., 2025; Visscher et al., 2025) with thick endocarps or hard coats), but seeds with thin coats can be significantly affected by the proteolytic conditions in the animals' digestive tracts and suffer reduced germination or even death (Santos et al., 2020; Trabelsi et al., 2023).

In endozoochory by fish, seeds passing through the digestive tracts of juvenile fish generally have a higher probability of germination, in comparison to those defecated by large fish, but there are deviations from this general pattern (Santos et al., 2020). Other studies reported seed viability in associations with genes and the functions of acid-pepsinogen-producing glands. Thus, the effects of gut passage through fish for seeds can be species-specific (Boedeltje et al., 2016). Nevertheless, the ability of fish to deposit seeds away from parent plants following consumption of fruits and seeds, and defecation, compensates for any reduced seed germinability and contributes to vegetation distribution and ecological dynamics within vicinity (Weiss et al., 2022). The biochemical and physiological mechanisms underpinning the survival of seeds following the gut passage of fish, mostly orthodox, is an under-researched topic.

Upon defecation, surviving seeds scattered undetermined distances away may have an advantage. They can also escape desiccation-induced death in the dung pats. The nutrients and leachates from the faecal materials, especially in the case of large mammalian droppings, may even promote the establishment of seedlings in some situations (Ramos et al., 2024). Otherwise, the abundance of seeds discharged in single droppings has inverse fitness consequences for plants.

Secondary dispersal of seeds in faeces carried out almost entirely by dung beetles will reduce spatial aggregation of seeds (Landim et al., 2022; Cheng et al., 2024; Lima et al., 2024). These arthropods also often bury the seeds while they feed their larvae with the dung, thereby protecting the seeds from detection and easy retrieval by other seed-eating animals, and even enhancing the growth of seedlings (Santos-Heredia and Andresen, 2014; Griffiths et al., 2016). In general, seed burial activities by dung beetles are more likely co-correlated with the seed trait (size) than desiccation sensitivity of seeds. An example is the burial of small seeds of Annona edulis (Annonaceae; desiccation tolerance unknown) by dung beetles while large seeds are left on soil surface following defecations by spider monkey and howler monkey (Santos-Heredia et al., 2010). With physical dormancy mostly overcome, the defecated seeds left on ground surface must germinate fast as risk hedging against subsequent predation or desiccation induced death.

5. Embryonic axis injury tolerance

When the physical defect in the seed is one that involves embryonic axis damage, it has been generally considered equivalent to seed death. For many seeds, hypocotyl or radicle injuries often result in germination failure even if the seeds are tolerant to pronounced cotyledon loss (Fukumoto and Kajimura, 2000). Nevertheless, there are exceptions where seeds withstand some loss of embryonic mass or location-specific embryonic damages (Cao et al., 2011).

5.1. Severity of embryonic axis damage

Some seeds with longer embryonic axes show better survival following partial embryonic damage. Among the desiccation sensitive oak seeds (acorns; Fagaceae), Quercus lobata and Q. agrifolia survive predation by terrestrial small mammals when the partly damaged embryonic axes are still attached to the cotyledons (Table 2; Perea et al., 2018). The germination potential and seedling development of these seeds with defective embryos are also comparable to those of the sound acorns. Such a valuable natural adaptation is inevitably necessary for population recruitment since the nutritious acorns are intensely predated by animals. However, injury to the plumule is mostly more critical than to the radicle. Plant regeneration of many Quercus spp. is unlikely when only the radicle survives and leaf development fails (McEuen and Steele, 2005; Zhang et al., 2014). Likewise, several members from the Clusiaceae family are also capable of demonstrating a similar growth potential from partially damaged embryonic axes that retain their proximal (plumule) parts. Orthodox seeds of Garcinia kola, recalcitrant seeds of Garcinia mangostana and seeds of Allanblackia parviflora, Garcinia gummi-gutta and Garcinia imberti having unknown desiccation tolerance have been reported to develop their seedlings from the seeds containing damaged radicles (Table 2; Lim, 1984; Joshi et al., 2006; Asomaning et al., 2011; Ofori et al., 2015; Seltzer et al., 2015; Anto et al., 2018). Thus, the polarity of the seeds in relation to the positional cue for shoot and root development success from seed fragments can be species and, sometimes, family-specific.

In more extreme situations, some small mammals completely remove the embryonic axes of seeds to halt or delay germination of non-dormant seeds enabling their storage as caches for future use (Xiao and Zhang, 2012). This behaviour of hoarding animals has frequently been reported for many oak species. The absence of embryonic axes makes the acorns act as "zombie seeds" with negligible loss of reserves over time when germination is disabled, allowing the animals to preserve the seeds (nutritionally) potentially for months (Steele, 2008). Tropical seeds of Carapa procera (Meliaceae; recalcitrant) are also treated in this way by the acouchies during the preceding fruit season to survive subsequent periods of food scarcity (Jansen et al., 2006). However, successful germination and plant recruitment happen when these foraging animals perform imperfect extirpation of the embryonic axes within seeds and forget their caches, exhibiting the persistence of seeds to thrive despite embryonic axis injuries (Xiao et al., 2013). Otherwise, the animals will actively manage such food supplies and have timely and repeated intervention of subsequent sprouting to minimize reserve depletion as the seeds thrive despite embryo injuries.

5.2. Atypical multi-seeded fruit

Some plant species have atypical reproduction within a crop load where a very small percentage of fruits are multi-seeded and bear multiple embryos in contrast to the regular fruits. These rare fruits are analogous to polyembryonic seeds, and some seeds may by chance avoid damage by larvae or seed gnawing animals; the escaped seeds within the fruits can germinate and develop into healthy seedlings. This phenomenon has been noted with some Scheelea (Arecaceae; desiccation tolerance unknown) and Quercus (Fagaceae; recalcitrant) species (Bradford and Smith, 1977; McEuen and Steele, 2005; Tu et al., 2025). The seed mortality rate of multi-seeded fruits is, therefore, inversely proportional to the number of seeds within the fruit.

6. Regenerative cotyledon

While biotic seed dispersal puts the regeneration integrity at risk as in Fig. 1, little is known of the natural capability of seed tissues to support entire plant development other than via intact embryos (i.e., radicle-hypocotyl-epicotyl-cotyledon) at post-embryogenesis. However, the growth ability from non-intact embryos has been revealed as an interesting adaptation in some seed-granivore interactions. In this case, full plants develop from seed fractions devoid of plumule–radicle axis. Compared to animal cells, plant cells have a greater degree of plasticity in tissue regeneration (Gordon et al., 2009; Chandler, 2011; Qi et al., 2014; Soyars et al., 2016). In vitro experiments have often shown juvenilization of differentiated cells followed by new cell formation and development into tissues and organs of different origins, and even full plantlets. It is the concept of organogenesis which is supported by the fundamentals of totipotency as directed by molecular signals and physiological responses (Greb and Lohmann, 2016). Imposing wounds during propagation from leaf and stem cuttings is one of the stimuli that triggers new cell initiation (Ikeuchi et al., 2016; Xu and Hu, 2020). The proliferation of embryogenic cells following tissue injury involves numerous complex physiological and biochemical changes, including the spatially and temporally coordinated hormone production at the cut sites (Wang et al., 2014; Chandler and Werr, 2015; Strader and Zhao, 2016). The reserve abundance and nutrition in the plant part or seed fraction may also influence the aptitude for new cell formation and differentiation into certain organs (Verdeil et al., 2007).

6.1. Cotyledonary cell-stemness

Cotyledon as a regenerative component in the seed has been noted, particularly by cell and tissue culture techniques, but such proliferation achievement does not always happen spontaneously in the natural environment (van Wyk and Botha, 1984; Silva and Pinheiro, 2009; Amadar and Barbedo, 2015). Diversity that exists throughout the plant kingdom and the enormous variation in cotyledon development and phenotype have partly been linked to cell stemness in the cotyledons of certain plants in the tropics, for example, in Eugenia spp. (Myrtaceae; recalcitrant) (Delgado et al., 2022). On the basis of comparative biology, cotyledon cell stemness has been demonstrated through the development of regenerative cells and the maturation of these cells will result in distinct growth and potentially full plant production (Fig. 1).

Seeds of several dicotyledonous plants from tropical rainforests which suffer heavy animal consumption have shown the ability to root and even produce entire plants from cotyledons following fragmentation (Table 2; Harms et al., 1997; Harrington et al., 2005). Regenerative cotyledons could be an evolved adaptation to ensure the population distribution of these plant species despite partial losses of tissue, especially the embryonic axes, regardless of seed size. Gustavia superba (Lecythidaceae; recalcitrant) in Central America, was one of the earliest noted species with the capability to regenerate entire plants from its large cotyledons (Table 2; Harms et al., 1997). Cotyledonary portions detached by predators have demonstrated a high probability of sprouting in moist growth medium on the forest ground. Under controlled conditions in laboratories and greenhouses, fractions cut deliberately from intact seeds have similar sprouting potential (Dalling and Harms, 1999). It is possible that meristematic tissues other than zygotic root and shoot exist within these large cotyledonous seeds, adding to the benefits that correspond with the reserve effect theory.

The seed of Idiospermum australiense (Idiospermaceae; recalcitrant; Franks and Drake, 2003) in the natural forest of north Queensland, Australia, is also capable of producing multiple independent plantlets from its starchy cotyledons (Table 2; Edwards et al., 2001; Edwards and Gadek, 2002). However, the necessity for having such regenerative potential in this large seed seems less critical to surviving animal consumption stresses as the predominant toxic alkaloids in the seed exclude faunal interactions. Thus, its diaspore, weighing up to 225 g each, establishes clumped young plants in the vicinity of the parent tree, deterring its spread in the ecosystem.

Relatively recent experiments that indicated cell stemness in seeds of Myrtaceae, especially Eugenia spp. (recalcitrant), is thought as a strategy for coping with high levels of physical damage caused by larval infestations and small mammal or fish consumptions in view of the thin seed coats covering them (Table 2; Delgado et al., 2010; Teixeira and Barbedo, 2012; Calvi et al., 2017). Members of this large family of flowering plants display considerable taxonomic differences and consist of a heterogenous assemblage of species exhibiting diverse seed traits (Ribeiro et al., 2021). In the context of embryogenesis, the seeds from Myrtaceae are broadly segregated as the eugenoid type, which contain a single embryo, and the multi-embryonic type. The eugenoid seed is a unique form where two partly fused cotyledons are filled with parenchymatous and meristematic tissues whilst its embryonic axis is invisible or microscopic (van Wyk and Botha, 1984). A similar morphological adaptation is evident in Vitellaria paradoxa (Sapotaceae; recalcitrant; Daws et al., 2004) such that the near indistinguishable axis is at the proximal end of the large cotyledons (Abdulai Iddrisu et al., 2019). Despite being monoembryonic, eight species of Eugenia (E. candolleana, E. stipitata, E. uniflora, E. involucrata, E. pruinosa, E. pyriformis, E. astringens, E. cerasiflora) simply form two normal plantlets when some seed parts are separated naturally or whole seeds are cut intentionally to mimic fragmentation by predators in nature (Table 2; Delgado et al., 2010; Teixeira and Barbedo, 2012; Amadar and Barbedo, 2015; Prataviera et al., 2015; Calvi et al., 2017; Alonso et al., 2019). Consequently, higher full plant regeneration rates can be attained compared to the uncut seeds, representing efficiency gains during plant propagation. Within the same family, seeds of Syzygium spp. also tend to be recalcitrant (11 species records in SID; Table 2; Tsan and Awang, 2021). Syzygium fibrosum, S. kuranda, S. gustavioides, S. malaccense and Myrcianthes coquimbensis possess distinguishable radicle-hypocotyl structures but display also totipotency in their cotyledons (Table 2; Harrington et al., 2005; Loayza et al., 2015; Nur Marini Fatini et al., 2024). Past research work has witnessed the development of entire plants from the cotyledons of cut seeds that contained no embryo axis. Apparently, somatic embryonic cells are haphazardly induced in the storage cotyledons following injury which contrasts with the polarity shown by the intact seeds. Regeneration of more than one entire plant from a monoembryonic seed in the family Myrtaceae and its association with known polyembryony within the family is yet to be studied.

For in vivo sprouting from the cotyledon of Eugenia, there is a self-inhibition effect where the initiation of new cells in the cotyledon is only possible after discarding the portion that contains the embryonic axis whilst an intact seed forms only one seedling (Amadar and Barbedo, 2015). The development of a plantlet has been suggested to be a hindrance to the concurrent formation of any full plant or new root. Thus, a seed will only exhibit the potential of multiple plant regeneration from its split fractions.

6.2. Injury- or incision-induced adventitious rooting (non-regenerative cotyledons)

Initiation of new cells from the cotyledon following wounding or incision on a seed can bring about rooting that is unaccompanied by shoot development (Harrington et al., 2005; Tsan, 2023). These cells that give rise to only a certain type of tissue or organ are pluripotent stem cells which do not have the ability of forming an embryo or entire plant. Thus, some seed fractions following animal predation show only rooting but fail to develop their shoots, depending on probably the polarity within the seeds.

In the unique Garcinia-type seed germination, the root emerges first at one end of the seed and the growth of the shoot occurs at the other end (Table 2; Lim, 1984; Mohd Noor et al., 2016). Then, a new root emerges from the base of the shoot, which is believed to be regenerated from the hypocotyl. This natural sprouting phenomenon itself is a clue to the existence of meristematic tissues in different positions of the seed. However, this kind of seed only develops full plants from regions that contain the regenerative or embryonic cells whereas other meristematic parts in the seed only achieve rooting success without any growth of shoot (Joshi et al., 2006; Asomaning et al., 2011; Anto et al., 2018).

For the apomictic Garcinia mangostana (Clusiaceae; recalcitrant) seed that has no distinctive plant-to-be structure, both cotyledons have meristematic tissues. The microscopic broad-based and irregularly-shaped integumentary bud located at random in the cotyledons is capable of developing an entire plant, but only adventitious roots are formed spontaneously from cut surfaces of detachment that do not contain any embryonic bud (Table 2; Lim, 1984; Mohd Noor et al., 2016). The indiscriminate embryogeny and, occasionally, the development of more than one integumentary bud in the seed are believed to be a survival strategy since the seed with its thin coat is easily shattered when the soft, juicy and delicately flavoured flesh that adheres tightly to it is predated. However, the seed is unpalatable because of the spread of tanniniferous cells on its covering.

Knowledge on the in vivo plant regeneration from cotyledons and seed tissues other than radicle-hypocotyl equivalents is limited (Lee, 2023). The regenerative potential of the different spatial zones in the seeds is yet to be supported by detailed physiological and histological evidence. Since in vitro cell differentiation into shoot and root and plantlets can be regulated by the application of auxins and cytokinins, the natural occurrence of these phytohormones or change in hormone balance, or sensitivity in seeds following injury, may regulate shoot and root development (Chickarmane et al., 2012; Anandan et al., 2018). Physical damage that initiates the intercellular communications and signalling via specific molecules, affecting cell fate, is another research subject that needs further investigation, particularly in recalcitrant seeds discussed above.

7. Seedling establishment

Development of normal seedlings from damaged seeds appears to offer adaptive advantage and to better ensure adulthood success. In the case of insect attack, accelerated germination of the predated seeds provides competitive conditions that outrun larval development (Talonia et al., 2022). Likewise, Quercus suber and Q. mongolica gain benefits from animal gnawing which reduces mechanical barriers and triggers speedy germination, followed by the growth of the seedlings (Ollerton and Lack, 1996; Branco et al., 2002; Yi et al., 2015). The accelerated seedling development also enables earlier assimilate synthesis and a higher chance of progressing to adulthood (Xia et al., 2011; Piiroinen et al., 2017). Rapid germination, despite loss of a great portion of the cotyledons, has also been suggested as a strategy to transfer nutritional reserves into indigestible and robust roots and shoots to avoid further predation since the seedling is less palatable compared to the seed (Yang and Yi, 2012; Leiva and Díaz-Maqueda, 2016; Tu et al., 2025).

In the natural environment, defective seeds tend to produce seedlings with reduced vigour in accordance with the reserve effect hypothesis (Janzen, 1976; Green and Juniper, 2004; Hou et al., 2010; Chen et al., 2025). Physiologically, heavily consumed seeds with little reserves left generally develop seedlings with lower photosynthetic rates, mineral nutrition and growth of roots and shoots (Yi and Zhang, 2008; Zhang et al., 2011), although they may not differ from those emerged from sound diaspores in their architectural proportions, for example root: shoot ratio (Branco et al., 2002; Perea et al., 2018). In other cases, large-seeded Quercus spp. that lost up to a quarter of reserves developed seedlings with insignificant shoot height, basal stem diameter, number of leaves, leaf area per plant, specific leaf area and biomass in comparison to the sound seeds; in contrast, subsequent reduced growth rates of the seedlings were obvious for the small-seeded seeds following mass loss (García-Hernández et al., 2023; Luo et al., 2023). Some seedlings emerging from the embryo-damaged seeds can also contain secondary metabolites and antioxidant constitutions that mediate antagonistic interactions, presumably as a protection response against herbivory (Perea et al., 2018).

Like intact seeds, the overall fate and fitness of seeds with physical defects in plant regeneration events also depend on the suitability of the site where they are deposited. In natural habitats, the major cause of seedling mortality is low soil moisture or lethal drought shortly after germination. Light regime is another critical factor that affects survival and growth of the new emergent, at the transition from the heterotrophic to autotrophic phase (Baraza et al., 2010; Sangsupan et al., 2018). After the reserves in the endosperm or cotyledons are depleted, rhizosphere chemistry becomes more important for the subsequent growth and development of seedlings (Mancilla-Leytón et al., 2013). The recovery of seedlings from seed predation effects is often greater in moist and nutrient-rich environments as compared to environments limiting the establishment of the seedlings. Nonetheless, the survival probability and growth from seeds in different environments are species-specific regardless of physical injury of seeds; climax species need the dim but humid continuous forest surroundings to thrive, at least in their early years, whilst pioneers flourish better in fragmented forest and canopy gaps where the seedlings receive higher light penetration (Bruna, 1999; Piiroinen et al., 2017). In relation to the resource needs, a common modulative or modificative response to habitats where growth factors are limiting is the conservative growth of the seedlings (Welker and Menke, 1990). Hence, the seedlings developed from damaged seeds often invest more assimilates in their roots at the expense of shoots, particularly when faced with moisture and nutrient deficits. Such a response is a necessity for recalcitrant seeds given the sensitivity of the seed to drying out (Pritchard et al., 2022).

Subsequent herbivory of the new and tender seedlings is a further pressure on natural plant regeneration. Seedlings with the capability of surviving and even recovering from folivore browsing are obviously at additional selective advantage over those that cannot (Barrere et al., 2024). The response of re-sprouting from stems after shoot browsing is a bet-hedging strategy for tolerating herbivory. The re-sprouting hypotheses are that the seedling should have dormant buds or meristematic tissues to support re-growth (Harms and Dalling, 1997; Yi and Liu, 2014; Pausas et al., 2016). With the loss of shoots to folivores, the seedlings will also need adequate reserves of non-structural carbohydrates in the cotyledons or roots for shoot re-growth (Dalling and Harms, 1999). Generally, a lower percentage of the seedlings with consumed cotyledons re-sprout as compared to those developed from the sound seeds (Bonfil, 1998; Gelviz-Gelvez et al., 2017). Externally, conducive factors of adequate moisture, light and nutrients on the site, as discussed above, exert additional selective influence and contribute to risk hedging against future resource deficits for the predated seedlings, although not necessarily through to adulthood (Zeppel et al., 2015). The ability of the new emergent to re-grow after herbivory is, however, one of the less investigated topics in plant science.

8. Future work

Germination following dispersal and predation is an adapted form of plant regeneration to sustain population growth. Animals as both the biotic dispersing vectors and consumers are planters that regulate the natural spatial pattern of plant species and maintain vegetation structure. In the seed-animal interactions, seeds evolve in terms of size, protective covering, bioactive compounds, including those involved in minimizing microbial infestation following injuries, and regenerative ability, while granivores of invertebrates and hoarding animals modify their seed selection and handling behaviours, thus enhancing the strength of the relationships. While a biologically diverse environment supports the predators of granivores as well, especially the tropical forests, the overall ecosystem and seasonal factors in combination may confer mixed effects on seed germinability and seedling performances post-predation.

In light of the fact that defective seeds are among the essential resources in natural plant recruitment, detailed field studies as well as controlled simulation work are needed to comprehend the damage tolerance limitations, including cell stemness, particularly in recalcitrant seeds. Research data that integrate the geographical differences into the role of preyed-upon seeds in natural population growth will add significance to the existing knowledge pool. Research work that also synchronizes the plant phenology and animal developmental stages, especially those of the invertebrates with relatively shorter life cycles, can have remarkable importance in interpreting the plant-animal mutualism niches for plant regeneration accomplishment in an ecosystem.

In the context of seed biology, the molecular biology and physiology of the regenerative tissues in seeds as triggered by predation remain less explored. We also lack data regarding the nutrition translocation and assimilate partitioning in the seeds that thrive despite animal consumption. Regenerative capabilities in the seed and seedling tissues in relation to hormonal concentrations and sensitivity and gene expression changes following herbivory should also be studied as plausible explanations for plant seed totipotency.

Acknowledgements

Fui Ying Tsan was supported by funding from Universiti Teknologi MARA [500-BPD(BKK.14/5/4) (188427)]. Louise Colville and Hugh W. Pritchard thank the Garfield Weston Foundation Global Tree Seed Bank Programme for support. Hugh W. Pritchard acknowledges funding from the Chinese Academy of Sciences, Kunming Institute of Botany project on 'Seed biology on important species of Magnoliaceae, Euphorbiaceae, Acanthopanaceae, Orchidaceae and Lauraceae', and the Government of China, Ministry of Science and Technology (MOST) for 'MOST's senior foreign experts introduction plan project'. The Royal Botanic Gardens, Kew, receives grant-in-aid from Defra.

CRediT authorship contribution statement

Fui Ying Tsan: Writing – review & editing, Writing – original draft, Visualization, Resources, Project administration, Investigation, Funding acquisition, Conceptualization. Louise Colville: Writing – review & editing, Visualization, Conceptualization. Hugh W. Pritchard: Writing – review & editing, Resources, Project administration, Funding acquisition, Conceptualization.

Declaration of competing interest

The authors declare no conflict of interest in this work.