A review of plant phenolics and endozoochory

Abstract

Phenolic compounds (phenolics) are secondary metabolites ubiquitous across plants. The earliest phenolics are linked to plants' successful transition from an aquatic to a terrestrial environment, serving as protection against damaging ultraviolet (UV) radiation, and as antioxidants to reduce oxidative stress in an atmosphere with an increasingly high O₂:CO₂ ratio. In modern plants, phenolics are best known for the defense against fungal and bacterial pathogens and as antifeedants that deter herbivory. Phenolics also play a role in seed dormancy, delaying germination, and lengthening viability in the seed bank. Many plants' seeds are endozoochorous – dispersed by animals, like birds, who eat and later excrete the seeds. Plants send visual signals to attract birds with UV‐sensitive (UVS) vision for pollination and seed dispersal. As fruits ripen, antioxidant activity and phenolic content decrease. The waxy cuticle of fruits increases in UV reflection as phenolic rings, which absorb UV light, degrade. The UV contrast that birds detect may act as an honest signal, indicating nutritional changes in the fruit. However, there is little evidence to support the evolution of UV coloration during ripening being driven by frugivore selection. Antioxidant properties of fruit phenolics may be dually adaptive in plants and avian frugivores.

INTRODUCTION

This paper underscores the ecological and evolutionary importance of phenolic compounds. By exploring their multifaceted roles in plants, this research highlights how phenolic compounds have influenced adaptation to a terrestrial environment, defensive strategies against herbivory and pathogens, and reproductive success including seed dispersal and germination, contributing to the resilience, and adaptability of plant species. This study examines the interaction between plants and their animal dispersers. Focusing on endozoochory, we explore how phenolics factor in by attracting dispersers and the effects of animal digestion on seed germination. We investigate the evolutionary and ecological relationship between today's predominant frugivores, birds, and fruit signaling strategies which may have coevolved with the ability of birds to see in the ultraviolet spectrum.

AN OVERVIEW OF PHENOLICS

Phenolic compounds, hereafter phenolics, are one of the three major classes of secondary metabolites which are chemical compounds found in plants that are not directly involved in primary metabolism (e.g., photosynthesis, respiration, etc.) (Taiz & Zeiger, 2006). Phenolics are ubiquitous within the plant kingdom but uncommon in bacteria, fungi, and algae. The nearly 10,000 different phenolics are united by the presence of an aromatic ring with one (phenol) or more (polyphenol) hydroxyl functional groups (Vuolo et al., 2019). Plant phenolics naturally arise from one of two pathways: the shikimate/phenylpropanoid pathway or the “polyketide” acetate/malonate pathway (Lattanzio et al., 2009). Phenolics can be divided at the molecular level into subgroups based on the construction of their carbon skeleton, kind of substituent, and degree of polymerization (Waterman & Mole, 1994). Subgroups include the simple phenolic compounds (simple phenolics and phenolic acids), the polyphenols (flavonoids and tannins), and others (stilbenes, lignans, and lignins) (Al Mamari, 2021). The flavonoids are further divided into anthocyanins, flavones, flavonols, and isoflavones (Table 1; Taiz & Zeiger, 2006).

TABLE 1 Phenolic compounds in seeds.

Classes	Example of abundant seed phenolic compounds	Functions and effects in seeds	References
Coumarins		Coumarin, 1,2-benzopyrone, fraxetin, isofraxidin	Antifeedant, pathogen defense, germination inhibitor	Abenavoli et al. (2006), Brooker et al. (2008), Matos et al. (2015), Mustafa et al. (2018), and Yin et al. (2014)
Stilbenes		Resveratrol, transresveratrol, piceid, viniferin, pterostilbene	Antioxidant, pathogen defense	Counet et al. (2006), Hasan & Bae (2017), and Nayak et al. (2019)
Flavanoids	Flavanols	Quercetin, quercetin-3-O-rhamnoside, kaempferol-3-O-rhamnoside, myricetin	Antioxidant, embryo protection, seed dormancy, pathogen defense	Debeaujon et al. (2000), Figueroa et al. (2018), Lepiniec et al. (2006), MacGregor et al. (2015), and Singh et al. (2017)
	Anthocyanins	Cyanidin, delphinidin, malvidin, peonidin, pelargonidin	Antioxidant, pigmentation, pathogen defense	Shirley (1998) and Singh et al. (2017)
	Isoflavones	Daidzein, genistein, glycitein, sissostrin	Antioxidant, pathogen defense	Corso et al. (2020), Lee et al. (2017), Shirley (1998), Singh et al. (2017), and Xu et al. (2019)
	Flavones	Apigenin, luteolin, isoorientin, diosmetin	Antioxidant	Corso et al. (2020), Figueroa et al. (2018), and Singh et al. (2017)
	Flavanones	Naringenin, sakuranetin, hesperitin, chalcone, eriodictyol	Antioxidant	Figueroa et al. (2018), Guerrero-Castillo et al. (2019), and Singh et al. (2017)
	Flavan-3-ols	Catechin, epicatechin, epigallocatechin, gallocatechin, proanthocyanidins, procyanidins, prodelphinidins, procyanidin dimers/trimers/pentamers	Pigmentation, germination inhibitor, seed dormancy, pathogen defense, antifeedant, antioxidant, embryo protection	Corso et al. (2020), Figueroa et al. (2018), Shirley (1998), and Singh et al. (2017)
	Flavan-4-ols	Phlobaphenes	Antioxidant, seed maturation, pathogen defense	Lepiniec et al. (2006) and Shirley (1998)

The phenological and spatial patterns of phenolics are complex; in a single species, it can be different between developmental stages, individuals, or populations. To properly function, phenolics accumulate in specific tissues or cell types where subcellular localization is highly regulated (Lattanzio et al., 2009). Phenolics are often transported from source cells to other nearby cells and sometimes sent to distant tissues or organs. There is significant compartmentalization of phenolics with accumulation occurring in the vacuoles of spongy cells (Santiago et al., 2000), covalently linked to the cell walls (Iiyama et al., 1994), in waxes (Schmutz et al., 1993), and other external surfaces (Cuadra & Harborne, 1996).

THE EARLY ROLE OF PHENOLICS IN PLANTS

Plants and their phenolics evolved together. Charophyceae and Chlorophyta, green algae likely to be the ancestor of land plants, possess sporopollenin which is linked to acetolysis-resistant phenolics in modern angiosperms (Stafford, 2000). Bryophytes, often considered the first land plants, have flavonoids, flavones, and lignans. Flavonoids, water-soluble polyphenols with 15 carbon atoms, occur in approximately 60% of mosses (Bryophyta) and liverworts (Marchantiophyta) (Markham, 1990). Flavones, a subgroup of flavonoids, are widely distributed among mosses and liverworts (Markham et al., 1998). The same lignans found in liverworts and hornworts (Anthocerophyta) are present in modern vascular plants along with a broad range of phenolics with differences among woody and herbaceous plants (Stafford, 2000).

The earliest phenolics are strongly linked to the transition from an aquatic to a terrestrial environment (Delaux et al., 2012). Living on land meant increased exposure to harmful UV and visible radiation (Cheynier et al., 2013). Just like sporopollenin in green algae that protects against UV radiation (Xiong et al., 1997), simple phenolics and flavonoids in early land plants may have been crucial as UV-B (280–320 nm) absorbing filters (Waterman & Mole, 1994). Another result of moving to land was exposure to an atmosphere with an increasingly high O₂:CO₂ ratio. Thus, plants needed a method of reducing oxidative stress. As a result, aerobic metabolic processes produced more reactive oxygen species (ROS) (Apel & Hirt, 2004; Igamberdiev & Lea, 2006). In tandem, an increase in the diversity and complexity of secondary metabolites (Graham et al., 2004) led to phenolics with strong antioxidant properties (Cooper-Driver & Bhattacharya, 1998) able to detoxify harmful ROS and alleviate oxidative stress (Chaki et al., 2020; Sakihama et al., 2002). It is the multifunctionality of phenolics that has made them influential in the success of modern plants (Table 1; Karabourniotis et al., 2014).

PHENOLICS AS HERBIVORE DETERRENTS

Perhaps the most well-known function of plant phenolics is for defense against herbivores and pathogens. Unlike animals, plants are sessile and cannot escape from biotic and abiotic stressors. Being linked to the ground means they must create metabolic products to survive attackers because escape is not an option (Taiz & Zeiger, 2006). Allocating resources to secondary metabolism is antagonistic to primary metabolism – a choice of grow or defend (Herms & Mattson, 1992). This means investing photosynthetic products into growth should be mutually exclusive of defense (Karabourniotis et al., 2014) and explains the negative correlation between a plant's photosynthetic ability and phenolic concentration (Sumbele et al., 2012). Balance is determined by an environment's unique combination of competition and herbivory that favors carbon allocation towards levels of growth and defense (Herms & Mattson, 1992). The fitness costs of defense may be more complex than the diversion of limited resources from growth and reproduction. A meta-analysis by Koricheva (2002) found that the interactions between plants and their environment (e.g., competitors, pollinators, different types of herbivores, abiotic stresses, and natural enemies) may play a significant role in the fitness cost of defenses. Despite the trade-off of investing in defense, phylogenetic patterns indicate the evolutionary trend in angiosperms towards increasingly toxic phenolics (Harborne, 1990). Over time, as plants have diverged they have acquired a greater number of defensive compounds belonging to more diverse chemical pathways, making it harder for herbivores to adapt to them (Becerra et al., 2009).

There is a wide array of defensive capabilities among phenolic subgroups (Taiz & Zeiger, 2006). Phenolics are produced as part of normal plant development and in response to physical damage (Pratyusha, 2022). Due to its physical rigidity and chemical durability, lignin deters most animals by making the plant indigestible (Jung & Allen, 1995). Lignification is a common response to microbial disease and can prevent pathogens from spreading (Vance et al., 1980). Phenolic acids and flavonoids that function as antioxidants in a healthy plant can become harmful prooxidants to insects by causing oxidative damage to their tissues (Grace, 2005). Phytoalexins are antimicrobial isoflavones produced after bacterial or fungal infection that likely defend against pathogen development (Hammerschmidt, 1999; Keen, 1981). Tannins are antifeedants that repel herbivory due to their general toxicity, decreasing protein digestion in vertebrates and increasing the production of ROS in insects (Barbehenn & Constabel, 2011). The outer cell layers of fruits often have high tannin concentrations, deterring herbivory until concentrations decrease with enzyme activity during ripening (Goldstein & Swain, 1963; Zarei et al., 2011). Tannins also defend against fungal and bacterial decay, with localization in nonliving heartwood (Scalbert, 1992).

Empirical studies provide insight into the antifeedant role of phenolics. Herbivores can select food sources based on the genetic variation in patterns of phenolics (Herms & Mattson, 1992). Potato cultivars with higher levels of phenolics have been found to be less attractive to invertebrate pests (Bennett & Wallsgrove, 1994). Similarly, bird pests are highly selective and avoid sorghum cultivars with high tannin levels compared to those without tannins (Butler, 1989). Chemical assays of crop tannin levels can be useful for farmers in predicting bird resistance (Hoshino & Duncan, 1982; McMillian et al., 1972; Tipton et al., 1970). In trees such as quaking aspen (Populus tremuloides), willow (Salix spp.), and balsam poplar (Populus balsamifera), younger shoots tend to have higher levels of phenolics (Lindroth & Hwang, 1996). Studies show snowshoe hares (Lepus americanus) and mountain hares (Lepus timidus) preferentially consume older shoots with the lower phenolic content and avoid relatively unpalatable juvenile shoots (Bryant, 1981; Reichardt et al., 1990; Tahvanainen et al., 1985). However, antifeedant capability is likely chemical-specific and not related to the total quantity of various phenolics present. Ruffed grouse (Bonasa umbellus) diets rely upon aspen buds and catkins during winter and spring. These herbivores have adapted to avoid antifeedant phenolics. Grouse selection of buds and catkins is towards those with lower levels of coniferyl benzoate, an ester formed by condensation of coniferol and benzoic acid (Jakubas & Gullion, 1991).

REGULATING SEED GERMINATION

Each seed contains an inactive embryo and germination is the beginning of its growth (Toole et al., 1956). During germination, respiration rapidly increases and involves several enzymatic pathways: glycolysis, the oxidative pentose phosphate pathway (OPPP), the tricarboxylic cycle, and oxidative phosphorylation (Botha et al., 1992). Dormancy is the period before viable temperate seeds germinate. Seeds can be prevented from germinating because of a physical barrier (coat-enhanced dormancy), because of the biochemical conditions within the embryo itself (embryo dormancy), or a combination of both (double dormancy) (Baskin & Baskin, 2021; Bewley, 1997). Dormancy serves an important role in protection from unsuitable conditions too harsh for seedling survival (Koornneef et al., 2002). Length of dormancy and timing germination is important among years as well as growing seasons because of high variability in stressors, such as competition and precipitation (Ten Brink et al., 2020).

Seed coats and embryos contain naturally occurring phenolics that affect dormancy (Lattanzio et al., 2009). Phenolics delay germination by suppressing enzymes involved in glycolysis (ALD and PGI) and OPPP (G6P-DH), disrupting cellular respiration (Gharachorloo et al., 2013; Muscolo et al., 2001). Phenolics also inhibit amino acid transport and protein synthesis (Van Sumere, 1972). Total phenolics increase after seed dispersal and degrade with time, suggesting an evolutionary mechanism that lengthens viability in the seed bank (Inácio et al., 2013). In addition to length of time, temperature affects phenolic degradation. Colder temperatures significantly decrease phenolic content and help explain why cold stratification is effective in germinating seeds (Willemsen & Rice, 1972).

In allelopathic plants, phenolics inhibit the germination of other competing plant's seeds (Williams & Hoagland, 1982). Phenolics leach into soil and inhibit seed germination by as much as 16–61% depending on which compounds and their concentrations (Muscolo et al., 2001). Additionally, these allelopathic chemicals can affect already established plants by modifying chloroplast and mitochondria membranes, preventing intracellular transport, and inhibiting the hydrolysis of ATP (Moreland & Novitzky, 1987). Not only are photosynthesis and respiration affected but cell membrane permeability, cell division, protein synthesis, and hormone activity are each affected by phenolic allelochemicals (Li et al., 2010).

ENDOZOOCHORY AND SEED GERMINATION

In nature, embryo dormancy is often overcome by exposure to cold temperatures during winter (summer annuals) or warm temperatures during summer (winter annuals) (Baskin & Baskin, 2004). Seed-coat dormancy can be broken, or scarified, either mechanically or chemically (Mousavi et al., 2011). Freeze–thaw cycles can physically break the seed coat (Kimura & Islam, 2012). Microbial activity can chemically scarify seed coats and enhance germination (Morpeth & Hall, 2000). Animals can provide physical and chemical scarification while acting as a seed transportation vessel.

Many extant plants (64% of gymnosperms and 27% of angiosperms) produce seeds that attract animal dispersers (Herrera & Pellmyr, 2009). Animal dispersal is particularly important in naturally fragmented habitats such as wetlands (Charalambidou et al., 2003). Understanding animal movement and their contribution to seed dispersal is increasingly important with anthropogenic pressures hindering plant dispersal (Tucker et al., 2021). Zoochory is the general term to describe any mode of animal dispersal. Epizoochory is dispersal by outside of the body, such as burrs stuck on fur (Iluz, 2011). Synzoochory is dispersal by seed-caching animals that do not consume the seed, such as squirrels (Sciurus spp.) burying acorns. Endozoochory is the purposeful ingestion of seeds, often involving a fleshy fruit surrounding the seed to entice the consumer. Endozoochory is the most widespread animal dispersal method of extant plants and can be considered the most genuine (Herrera, 1989). Endozoochory provides a means of scarification for seeds that are relatively small or have hard enough coats to withstand passage through digestive tracts (Krefting & Roe, 1949).

It has been long debated how effective animal guts are at scarifying dormant seeds. Early studies found that germination could benefit from passage through animal digestive tracts but was dependent on species of seed and animal consumers (Krefting & Roe, 1949; Swank, 1944). The notion that effectiveness is dependent on the animal consumer is supported by a variety of studies (Table 2). Prosopis flexuosa seeds consumed by herbivorous mammals (Dolichotis patagonum and Lama guanicoe) and tortoises (Chelnoidis chilensis) experienced significantly increased germinability whereas pampas fox (Lycalopex gymnocercus) and greater rhea (Rhea americana) ingestion had no noticeable effect (Campos et al., 2020). Black mulberry (Morus nigra), black bryony (Tamus communis), and red-berry mistletoe (Viscum cruciatum) seeds ingested by common blackbirds (Turdus merula) had significantly greater germination percentages than those eaten by white-spectacled bulbuls (Pycnonotus xanthopygos) (Barnea et al., 1991). Traveset and Willson (1997) found little variation in multiple seed species' germination rates after consumption by bird and bear digestive systems – only one plant, red elderberry (Sambucus racemosa), appeared to benefit more from the guts of varied thrush (Ixoreus naevius) than other animals. Some seeds experience more prompt germination at the expense of reduced viability. For example, cattle and rodent endozoochory enhance legume seed germination but decreases overall viability (Campos & Ojeda, 1997). It is important to note that germination may be less successful after animal consumption, furthering the notion that germinability is highly dependent on the plant and animal species involved (Charalambidou et al., 2005; Cosyns et al., 2005).

TABLE 2 Seeds tested with frugivore bird species/family, effect(s) of ingestion on seed germination rate (+, enhancement; —, inhibition; 0, neutral), fruit type (F, fleshy; D, dry), and seed size (S, small, <5 mm; M, medium, 5–10 mm; L, large, >10 mm).

Plant species (Family)	Disperser species	Disperser family	Effect(s)	Fruit type	Seed size	References
Anacardiaceae
Rhus glabra	Colinus virginianus	Odontophoridae	+	F	S	Krefting and Roe (1949)
Toxicodendron vernix	Colinus virginianus	Odontophoridae	+	F	S	Krefting and Roe (1949)
Toxicodendron vernix	Phasianus colchicus ssp. torquatus	Phasianidae	+	F	S	Krefting and Roe (1949)
Apocynaceae
Arum hygrophilum	Turdus merula	Turdidae	0—	F	S	Barnea et al. (1991)
Oplopanax horridus	Ixoreus naevius	Turdidae	00	F	M	Traveset and Willson (1997)
Oplopanax horridus	Turdus migratorius	Turdidae	00	F	M	Traveset and Willson (1997)
Caprifoliaceae
Lonicera tatarica	Dumetella carolinensis	Mimidae	0	F	S	Krefting and Roe (1949)
Lonicera tatarica	Turdus migratorius	Turdidae	+	F	S	Krefting and Roe (1949)
Sambucus canadensis	Dumetella carolinensis	Mimidae	+	F	S	Krefting and Roe (1949)
Sambucus canadensis	Turdus migratorius	Turdidae	+	F	S	Krefting and Roe (1949)
Sambucus canadensis	Phasianus colchicus ssp. torquatus	Phasianidae	−	F	S	Krefting and Roe (1949)
Sambucus racemosa	Ixoreus naevius	Turdidae	0+	F	S	Traveset and Willson (1997)
Sambucus racemosa	Turdus migratorius	Turdidae	0+	F	S	Traveset and Willson (1997)
Cornaceae
Cornus racemosa	Colinus virginianus		−	F	S	Krefting and Roe (1949)
Cornus racemosa	Phasianus colchicus ssp. torquatus	Phasianidae	−	F	S	Krefting and Roe (1949)
Cornus stolonifera	Colinus virginianus	Odontophoridae	−	F	S	Krefting and Roe (1949)
Cornus stolonifera	Phasianus colchicus ssp. torquatus	Phasianidae	−	F	S	Krefting and Roe (1949)
Ephedraceae
Ephedra campylopoda	Turdus merula	Turdidae	00	F	S	Barnea et al. (1991)
Ephedra campylopoda	Pycnonotus xanthopygos	Pycnonotidae	00	F	S	Barnea et al. (1991)
Ericaceae
Vaccinum alaskaense, V. ovalifolium	Ixoreus naevius	Turdidae	00	F	S	Traveset and Willson (1997)
Vaccinum alaskaense, V. ovalifolium	Turdus migratorius	Turdidae	00	F	S	Traveset and Willson (1997)
Liliaceae
Asparagus aphyllus	Erithacus rubecula	Muscicapidae	00	F	S	Barnea et al. (1991)
Asparagus aphyllus	Turdus merula	Turdidae	00	F	S	Barnea et al. (1991)
Streptopus amplexifolius	Ixoreus naevius	Turdidae	00	F	S	Traveset and Willson (1997)
Streptopus amplexifolius	Turdus migratorius	Turdidae	00	F	S	Traveset and Willson (1997)
Moraceae
Morus alba	Turdus migratorius	Turdidae	+	F	S	Krefting and Roe (1949)
Morus nigra	Turdus merula	Turdidae	++	F	S	Barnea et al. (1991)
Morus nigra	Pycnonotus xanthopygos	Pycnonotidae	++	F	S	Barnea et al. (1991)
Myrtaceae
Myrtus communis	Turdus merula	Turdidae	0+	F	S	Barnea et al. (1991)
Myrtus communis	Pycnonotus xanthopygos	Pycnonotidae	0+	F	S	Barnea et al. (1991)
Rhamnaceae
Rhamnus alaternus	Turdus merula	Turdidae	++	F	S	Barnea et al. (1991)
Rhamnus alaternus	Pycnonotus xanthopygos	Pycnonotidae	++	F	S	Barnea et al. (1991)
Rhamnus palaestinus	Turdus merula	Turdidae	+—	F	S	Barnea et al. (1991)
Rhamnus palaestinus	Pycnonotus xanthopygos	Pycnonotidae	+0	F	S	Barnea et al. (1991)
Rosaceae
Prunus serotina	Turdus migratorius	Turdidae	+	F	M	Krefting and Roe (1949)
Prunus virginiana	Phasianus colchicus	Phasianidae	−	F	M	Krefting and Roe (1949)
Rosa blanda	Colinus virginianus	Odontophoridae	−	F	S	Krefting and Roe (1949)
Rosa blanda	Phasianus colchicus	Phasianidae	−	F	S	Krefting and Roe (1949)
Rosa sp.	Tympanuchus phasianellus	Phasianidae	−	F	S	Krefting and Roe (1949)
Rosa sp.	Phasianus colchicus	Phasianidae	+	F	S	Krefting and Roe (1949)
Rubus occidentalis	Bombycilla cedrorum	Bombycillidae	−	F	S	Krefting and Roe (1949)
Rubus sanctus	Turdus merula	Turdidae	—0	F	S	Barnea et al. (1991)
Rubus sanctus	Pycnonotus xanthopygos	Pycnonotidae	—0	F	S	Barnea et al. (1991)
Rubus sp.	Bombycilla cedrorum	Bombycillidae	0	F	S	Krefting and Roe (1949)
Rubus sp.	Dumetella carolinensis	Mimidae	+	F	S	Krefting and Roe (1949)
Rubus sp.	Turdus migratorius	Turdidae	+	F	S	Krefting and Roe (1949)
Rubus spectabilis	Ixoreus naevius	Turdidae	0+	F	S	Traveset and Willson (1997)
Rubiaceae
Rubia tenuifolia	Turdus merula	Turdidae	0+	F	S	Barnea et al. (1991)
Rubia tenuifolia	Pycnonotus xanthopygos	Pycnonotidae	0+	F	S	Barnea et al. (1991)
Saxifragaceae
Ribes bracteosum	Ixoreus naevius	Turdidae	00	F	S	Traveset and Willson (1997)
Ribes bracteosum	Turdus migratorius	Turdidae	00	F	S	Traveset and Willson (1997)
Ribes missouriense	Bombycilla cedrorum	Bombycillidae	+	F	S	Krefting and Roe (1949)
Ribes missouriense	Dumetella carolinensis	Mimidae	+	F	S	Krefting and Roe (1949)
Vitaceae
Vitis riparia	Colinus virginianus	Odontophoridae	−	F	S	Krefting and Roe (1949)
Vitis riparia	Phasianus colchicus	Phasianidae	−	F	S	Krefting and Roe (1949)

It appears alien animals may decrease the germinability of seeds more than their native counterparts. In Argentina, invasive European wild boars (Sus scrofa) decrease the germinability of all seeds they consume (Campos & Ojeda, 1997). In the Galápagos Islands, native giant tortoises (Chelonoidis niger) significantly improve the speed and percentage of germination of native tomato seeds while no seeds germinated after consumption by invasive rats (Rick & Bowman, 1961). In the Canary Islands, the viability of Rubia fruticosa seeds is much greater after ingestion by native reptiles and birds than by exotic mammals like European rabbits (Oryctolagus cuniculus) and Barbary ground squirrels (Atlantoxerus getulus) (Nogales et al., 2005).

There is also debate over the effect of retention time, or how long it takes a seed to go through the digestive tract. Barnea et al. (1991) found seeds with longer retention times had increased seed coat permeability and therefore more successful germination. Likewise, Capparis spinosa seeds with longer retention times in lizard digestive tracts broke dormancy and increased germination rate (Yang et al., 2021). Alternatively, wigeon grass (Ruppia maritima) seeds ingested by five dabbling duck species were more likely to germinate if the retention time was shorter (Charalambidou et al., 2003). Campos et al. (2020) found that retention time was not the most important factor because, among five consumers, the species with a significantly longer retention time (Chelonoidis chilensis) did not have the lowest seed viability or germinability. Traveset and Willson (1997) also found retention time was unimportant for Alaskan native shrub and herb seeds.

It is more likely that the nature of physical and chemical treatment the seed experiences in the gut is more important than the time it takes to pass through (Schupp, 1993). A recent study by van Leeuwen et al. (2023) on waterfowl digestion found that species-specific viability was entirely dependent on the birds' gizzard, where foods are mechanically digested, whereas germinability was dependent on intestinal digestion. An extensive literature review of 366 plant species from 76 publications by Soltani et al. (2018) emphasizes the significance of the type of dormancy. Germination of all physically dormant seeds (coat-enhanced dormancy) improved after endozoochory regardless of size. This suggests animal digestion may decrease the seed coat phenolic content that would typically suppress germination.

AVIAN VISION: FORAGING USING ULTRAVIOLET SIGNALS

Birds, with few exceptions, rely on their ability to visually assess their surroundings more than any other terrestrial vertebrate (Jones et al., 2007). There are only a handful of extant birds where vision is not the primary sense, such as kiwis (Apteryx spp.) whose vision likely regressed in the absence of predation (Martin, 2007). High visual awareness helps birds to navigate surroundings, avoid predators, and assess potential mates. Their acute vision, particularly sensitivity in the near ultraviolet, is useful in foraging (Hart, 2001). For example, the first bird known to use UV visual cues for foraging was the common kestrel (Falco tinnunculus) which detects UV-reflecting scent trails of voles (Viitala et al., 1995). Although birds are sensitive to a broader range of light, their sensitivity to contrast between wavelengths is much less than that of humans. This means that there needs to be higher degrees of contrast for birds to detect detail while foraging for food (Martin, 2022).

The avian retina is generally more advanced and complex than that of humans (Husband & Shimizu, 2001). A bird's interpretation of color is different from ours and can differentiate between more wavelengths, giving them significantly greater spectral resolution (Martin, 2022). For most, this resolution is across a broad spectrum from ultraviolet (UV) to far-red light (Cuthill et al., 2000). UV vision is a general property of birds and is only absent in relatively few species (Goldsmith, 1990). This extended range is a result of colored oil droplets and an additional cone type for a total of 4 (tetrachromacy) compared to our 3 (Vorobyev et al., 1998). The few who have evolved towards decreased UV sensitivity may owe this difference to additional pigmentation in the eye lens, likely protecting against UV damage to the retina (Olsson et al., 2021).

Bird species sensitive to near UV light (300–400 nm) can be categorized into two classes based on the maximal sensitivity of their short-wave type 1 (SWS1) cones (Burns & Shultz, 2012). Species that have SWS1 cones with pigments with maximal sensitivity between 355 and 370 nm are classified as UV-sensitive (UVS) whereas those with maximal sensitivity between 405 and 420 nm are violet-sensitive (VS) species (Cuthill, 2006; Wilkie et al., 2000). Whether a species has UVS or VS vision is caused by a single amino acid substitution and is simple to determine through genomic sequencing of the SWS1 cone opsin gene (Ödeen & Håstad, 2013). VS species are not blind to UV light but lack the ability to distinguish between short wavelengths like UVS species (Emmerton & Delhis, 1980; Martin, 2022). The relatively low transmission of UV light in VS species is likely from the presence of UV-blocking pigmentation in the eye lens (Lind et al., 2014).

Plants can increase signaling success to birds by enhancing chromatic (wavelength-related) and/or achromatic (intensity-related) contrasts between fruits/flowers and their backgrounds (Schaefer et al., 2006). Phenolics help plants visually guide pollinators to flowers (Iwashina, 2003) and later attract animal consumers to fruits (Samanta et al., 2011). Anthocyanins are colored flavonoids responsible for most of the red, pink, purple, and blue plant coloration (Taiz & Zeiger, 2006). Almost all polyphenols can act as co-pigments, forming complexes with and changing the intensity or coloration of anthocyanins (Lattanzio et al., 2009). Distributions of flavonoids among flower tissues can create conspicuous patterns that help guide pollinators to nectar and pollen because they absorb UV light (Lunau, 1992). As fruits ripen, antioxidant activity and total phenolic content decrease (Castrejón et al., 2008). This decline in phenolics could explain why many fruits tend to reflect UV more after ripening (Cronin & Bok, 2016). There are exceptions to this trend. For example, as yew berries (Taxus baccata) ripen and change from green to red, UV reflectance declines (Cuthill et al., 2000).

Fruit color can act as an honest signal, allowing bird dispersers to increase their intake of vital nutrients and energy (Schaefer et al., 2014). Color change during ripening is considered an adaptation to attract seed dispersers (Valenta et al., 2017). Despite most bird-dispersed fruits being red or black in color, this coloration alone does not seem to produce a significant preference (Willson et al., 1990). The UV color of a fruit's waxy cuticles makes the fruit more conspicuous to a bird on the lookout for its next meal (Burkhardt, 1982) because common natural backgrounds like leaves, bark, and soil do not reflect UV (Chittka et al., 1994). This increased UV reflectance makes the fruit brighter overall and does not produce a specific UV hue (Willson & Whelan, 1989). On the contrary, if the fruit absorbs UV more strongly relative to its background, conspicuousness can also increase (Bennett & Cuthill, 1994). The UV contrast of fruit against backgrounds is often enhanced by secondary structures like bracts and stems (Schmidt et al., 2004).

The use of UVS vision for foraging is most well-known among frugivores. Fruits that reflect UV are strongly associated with the presence of UVS bird species (Rajchard, 2009). In Panama, a study by Altshuler (2001) showed that when a UV-absorbing filter was used, foraging birds removed less fruits from shrubs. Birds in temperate regions also show fruit preference based on UV cues. Lab experiments show redwings (Turdus iliacus) and black grouse (Lyrurus tetrix) prefer UV-reflecting blueberries (Vaccinium myrtillus) over non-reflecting blueberries under natural conditions but have no preference when UV illumination is absent (Siitari et al., 1999, 2002). Fish crows (Corvus ossifragus) are able to detect UV-reflecting blueberries from farther distances because of the fruits' increased intensity and color contrast with foliage (Schaefer et al., 2006). Eurasian blackcaps (Sylvia atricapilla) discriminate between the nutritional value (anthocyanin content) of fruits by selecting fruits based on their UV reflectance (Schaefer et al., 2008). In this sense, UV reflectance is an honest signal of nutrition since birds are actively selecting for higher anthocyanin content which is positively correlated with caloric value.

EVOLUTION OF FRUIT SIGNALS AND UVS VISION

Did preferences for UV-contrast in fruits among UVS species come about through coevolution between birds and angiosperms? Or are these preferences just selection on the birds' behalf through the course of avian evolution?

The exact origin of angiosperms remains a mystery to this day (Li et al., 2019). Paleobotanists generally agree that the diversification of extant angiosperm lineages evolved during the Late Jurassic and Early Cretaceous Periods approximately 150 million years ago (Mya) (De Bodt et al., 2005). More than 80% of extant angiosperm orders likely originated during an early burst of diversification in the Early Cretaceous known as “Darwin's abominable mystery” (Zuntini et al., 2024). During the first 70–80 million years of their evolution, angiosperms had small fruits and seeds (Crane et al., 1995). The most important dispersal agents for these early fruits were likely rodent-like mammals, the multituberculates, that are now extinct (Wilson et al., 2012). Significant diversification of angiosperm fruits began 80 Mya (Lupia et al., 1999) with rodents and primates taking over as the primary seed dispersers (Boyer et al., 2012; Collinson & Hooker, 2000). Diversification of fruit sizes and types peaked during the Eocene (55–50 Mya) (Eriksson et al., 2000). Flight became particularly advantageous after a climate shift around the Eocene–Oligocene boundary (34 Mya) which created patchy, semi-open woodland habitats with food sources farther apart (Graham, 1999). Bats and birds, specifically passerines, became the dominant frugivores during the Oligocene (34–23 Mya) and Miocene (23–5 Mya), exploiting an already diverse variety of fleshy fruits (Mayr, 2005; Teeling et al., 2005).

Tetrachromacy and UVS pigment are the ancestral condition of tetrapods, with separate losses of UV sensitivity in mammals, amphibians, and birds (Hunt et al., 2001). The ancestor of passerines is hypothesized to have had UVS pigment (Ödeen et al., 2011) with initial passerine divergence occurring 71–60 Mya (Ericson et al., 2002). Passerine diversification rates significantly increased during the Late Miocene (Oliveros et al., 2019). Today, passerines are the most common and widespread frugivores in the animal kingdom. Because tetrachromacy preceded the radiation of many angiosperms, it is likely that fruit color is an evolved attractant to birds (Valenta et al., 2017). Color of bird-dispersed fruits has experienced a stronger selection for conspicuousness than that of mammal-dispersed fruits (Duan et al., 2014; Lomascolo & Schaefer, 2010). Despite this, the Oligocene–Miocene “passerine take-over” was most likely not because of coevolution between birds and fruits. Passerines were able to exploit an existing niche under new conditions, but the fruits evolved through interactions with extinct mammals (Eriksson, 2016). It is clear the success of passerines was not only related to frugivory (Jønsson et al., 2011).

There is a general lack of evidence for the evolution of fruit color being driven by avian frugivore selection (Wheelwright & Janson, 1985). Flowers show strong coevolution with pollinators. Because the plant requires pollen to be taken to a conspecific, selection has been towards food-rewarding flowers that attract a narrow range of pollinators (Johnson & Anderson, 2010). Coevolution between frugivores and plants, however, is less likely. Fruits benefit from interacting with a large variety of frugivores (Schaefer et al., 2004). Similarly, frugivores consume many different fruits and their dependence on a particular species is insignificant (Herrera, 2002; Jordano, 2000). Therefore, fruit color is expected to converge towards similar coloration that can be easily detected by a wide range of animals (Valenta et al., 2015). Modeling fruit reflectance according to avian vision shows selection for increased detectability is not the primary driver of fruit color (Schaefer et al., 2007). Other selective pressures that may influence the evolution of UV-reflecting pigmentation include pathogen defense and reduction of desiccation (Schaefer & Schaefer, 2007). Phenolics may be selected for by frugivores and by fruits alike for their antioxidant properties (Schaefer, 2011).

CONCLUSIONS

The origin of phenolics in early land plants is closely tied to their ability to absorb UV light and antioxidant properties. As plants evolved, phenolics diversified, becoming important in defense against pathogens and herbivores. Phenolics are also involved in plant reproduction, regulating seed dormancy, attracting pollinators to flowers, and enticing seed dispersers with colorful fruit. Endozoochorous plant species benefit from attracting frugivores by movement and dispersal of seeds as well as increased germinability after passing through the animal digestive tract. Birds are perhaps the most common frugivores and use UVS vision to detect ripe fruit with their contrasting backgrounds. Changes in UV reflection as fruits ripen are linked to phenolic content in the fruits' waxy outer layers. However, it is likely that the evolution of UV-contrast in fruits is not due to coevolution with birds. Passerines exploited an existing niche of fruit-producing plants that evolved through interactions with extinct mammals. Coevolution between seed dispersers and fruits is less likely than between pollinators and flowers because plants benefit from interacting with an increasing variety of frugivores. Despite this, modern passerines often still appear to use UV cues that evolved long ago to select fruits based on phenolic content.

This review has highlighted new research opportunities and identified gaps in current scientific understanding. Most studies on fruit selection and the effects of endozoochory on seeds have been conducted in laboratory settings. Field studies could expand the ecological context of these interactions by considering factors such as climate, habitat, competitors, predators, and natural food sources. There is a significant lack of comprehensive data on the phenolic content in seeds dispersed by birds, particularly before and after gut passage. Examining the chemical content of seeds before and after endozoochory, alongside measuring germination rates, could provide more insight into which phenolics are most influential on germination and/or most sensitive to digestion. Lastly, there is limited understanding of the conservation implications of phenolic-mediated seed dispersal. The role of phenolics in attracting bird dispersers and their effect on germination could potentially influence the success of invasive and/or introduced fruit-bearing species, such as rosa multiflora (Liaudanskas et al., 2021).

AUTHOR CONTRIBUTIONS

Samuel A. Krebs: Conceptualization (equal); investigation (lead); project administration (equal); writing – original draft (lead). Michael L. Schummer: Conceptualization (equal); project administration (equal); writing – original draft (supporting).

ACKNOWLEDGEMENTS

We would like to recognize the generosity of the Friends of Montezuma Wetlands Complex, Seneca Meadows, Inc., Eaton Birding Society, and Rice Creek Associates for funding the research and development of this article. We would like to thank the following individuals for their contributions of critical review and commentary: Dr. Vadoud H. Niri, PhD. Associate Professor, Department of Chemistry, SUNY Oswego; Dr. Danilo D. Fernando, PhD. Associate Professor, Department of Environmental Biology, SUNY-ESF; Dr. Hyatt C. Green, PhD. Associate Professor, Department of Environmental Biology, SUNY-ESF.

CONFLICT OF INTEREST STATEMENT

The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.

DATA AVAILABILITY STATEMENT

This is a review article; all research papers used by the authors are included in the literature cited. No data sets were used by the authors.

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