Knowledge Gaps on the Effectiveness of Seed Dispersal by Mammals and the Effect of Human Disturbances: A Review

Abstract

Seed dispersal by frugivorous mammals is crucial for plant reproduction, but anthropogenic disturbances can disrupt this process. However, there is a lack of research on mammalian seed dispersal in anthropogenic habitats, with few systematic literature reviews available. In order to address this gap, a review of scientific literature published since 1990 was conducted. A total of 275 articles from 52 countries, predominantly from South America, were found for the review. These articles contained information on 764 mammal species from 54 families, with Canidae being the most studied. The studies focused on various aspects of seed dispersal, including animal visitation rates (60%), seed quantity in faeces (78.9%), seed viability (49.1%), germination (49.5%), and seedling recruitment. However, only a small percentage of the studies examined the impacts of human disturbance on seed dispersal (5.8%), particularly the quantity of seeds dispersed. There is a need for further studies that integrate the analysis of seed dispersal effectiveness by mammals while considering the effects of human disturbances, particularly in areas with high plant and mammal diversity threatened by human activities.

1. Introduction

Plant–animal interactions play a key role in maintaining biodiversity and ecosystem functioning [1,2]. Seed dispersal by frugivorous animals is one example, as the recruitment of many plant species depends on it [3]. In fact, at least 78% of woody plants in tropical and temperate forests require animals for seed dispersal [4,5]. However, not all frugivores fulfil their dispersal role in the same way [6,7,8,9,10]. Frugivores differ in their seed dispersal effectiveness, i.e., the number of new adult plants produced as a result of foraging and seed dispersal by the animal [11]. This is because seed dispersal effectiveness (SDE] is determined by the quantity and quality of seeds dispersed, which depends on the identity of the animals and plants and their respective behavioural, physiological and other characteristics [12,13]. The quantity of seeds dispersed is determined by the number of feeding visits of animals to plants, which may vary between species and individuals, and the quantity of seeds removed at each of these feeding visits. On the other hand, the quality of dispersal is strongly influenced by the viability of the seeds before they are handled by the animal and after they are consumed and defecated, including the dispersal distance and the location to which they are taken [12,13].

Intensification of human disturbances are affecting species diversity and abundance, leading to a biodiversity crisis [14,15,16,17]. A less visible aspect of this crisis is the loss of ecological interactions, which can lead initially to functional extinctions and ultimately to local and global extinctions [2,18,19]. The dispersal role of frugivores can be negatively affected by anthropogenic disturbances, which typically result in population declines [20]. Reduced population sizes may contribute to lower plant visitation rates and, consequently, to a reduction in the number of fruits removed by animals [21,22,23]. Numerous disturbances threaten biodiversity, among them, hunting, land use change due to agricultural and forestry expansion, or alien invasions. Mining is another menace whose effects on seed dispersal have not been widely assessed. Human impact growth determines the increased development of road infrastructure [24,25]. In this context, it is important to analyse the effect of roads on seed dispersal, plant regeneration and the overall dynamics of ecological communities [26]. A study analysing the dispersal service provided by rodents showed the negative impact of roads on the effectiveness of this mutualistic interaction, due to reductions in populations of these dispersers [27]. Another study found that the presence of roads did not prevent seeds from dispersing downslope and accumulating on edges with high vegetation abundance, but it did prevent seeds from being transported across them [28]. Introductions of plant and animal species also affect seed dispersal, and invasive species that spread rapidly and become very abundant may alter mutualistic relationships with native species, with unknown consequences for both populations and communities [29]. For example, Prunus mahaleb exhibits traits associated with successful invaders in the Argentine pampas, making it an attractive food source for generalist dispersers. These dispersers remove the pulp, increasing seed germination capacity, which is also high in semi-natural areas. This promotes successful recruitment even in fruits moved by dispersers that have seeds with low germination potential [30]. Global warming due to climate change has been addressed in studies of seed dispersal, where it has been found that in temperate regions, plants dispersed by mammals that make altitudinal movements allow fruits produced in spring and summer to have a high potential to escape high temperatures [31], while those consumed in autumn–winter are unable to escape [32]. This shows that seed dispersers help sort plants into their climatic altitude ranges [33].

The loss of habitat continuity (i.e., fragmentation) due to anthropogenic disturbances can reduce the ability of animals to move and, therefore, the likelihood of interacting with plants, as well as the distance over which seeds are dispersed and new seedlings recruited [34,35,36]. The rates of plant visitation and subsequent fruit removal by animals may also be influenced by the structure of habitat patch edges [13,37]. These edges can act as barriers to seed-dispersing animals, depending on the structure of the edges and the characteristics of the animals, such as body size [38,39]. Low vegetation cover edges facilitate the occupation of patches by seed-dispersing animals such as birds and foxes, allowing seed dispersal [40,41]. Edges with high vegetation cover and complex vegetation structure, such as crop margins, can facilitate higher abundances of small rodents [42,43], thus increasing the likelihood of seed predation [44,45,46]. Finally, habitat degradation through fragmentation and edge habitat creation can result in simplified habitat textures [47], which are often associated with changes in microhabitat conditions that can negatively affect seedling recruitment [48,49].

Many studies have focused on frugivory and seed dispersal by birds, and to a lesser extent by mammals [21]. Many of these studies have addressed various issues related to seed dispersal of individual species [40,50,51,52], such as fruit characteristics [52,53] or the effect of passage through the digestive tract of animals on the viability and germination of dispersed seeds [51,54]. Similarly, several studies have examined the effects of forest fragmentation and the direct effects of human disturbance, such as hunting and selective logging, on animal-mediated seed dispersal [53,55,56,57]. In previous reviews examining the effects of fragmentation and selective logging on seed dispersal, it has been concluded that habitat fragmentation has a weaker negative effect on animal-mediated seed dispersal than selective logging [21]. Another study reached a similar conclusion when examining the effects of habitat alteration on bird guilds [58]. Although these studies have contributed significantly to our knowledge, extrapolating species-level effects to broad taxonomic categories remains a difficult task, as many species may respond differently depending on the type of disturbance and habitat [59]. To date, no studies have examined how the components of mammalian seed dispersal effectiveness vary and how anthropogenic disturbance affects this process. Consequently, it is largely unknown whether different groups of seed-dispersing mammals respond differently to habitat fragmentation and degradation, and how their seed dispersal effectiveness varies.

We hypothesize that the effectiveness of dispersal mediated by frugivorous mammals is negatively affected by human disturbance. We, therefore, predict that in disturbed environments, there will be (i) a decrease in visitation rates, (ii) a reduction in the number of seeds dispersed by the animals, (iii) a neutral effect on seed viability, because this factor depends on physiological characteristics of the animals that are not expected to be negatively impacted by disturbances, and (iv) a decrease in seedling recruitment. The general aim of this review is to assess the state of knowledge about the effect of anthropogenic disturbances on the effectiveness of seed dispersal by mammals. The specific objectives are to understand how human disturbances affect the components (quantity and quality) and subcomponents (visitation rate, seed quantity, viability, and germination) of global mammalian seed dispersal effectiveness.

2. Materials and Methods

2.1. Literature Search

We conducted a systematic search for peer-reviewed articles published since 1990 and up to March 2024 on mammalian endozoochory seed dispersal. We reviewed articles within two peer-reviewed scientific literature databases, SCOPUS, www.scopus.com (8 October 2024) and WOS, https://www.webofscience.com/wos/woscc/basic-search (10 October 2024). For the searches, we used the following terms (in full article, article title, abstract and keywords): ‘mammal’ AND ‘diet’ OR ‘endozoochory’ OR ‘seed dispersal’ OR ‘effectiveness’ OR ‘frugivory’ OR ‘fragmentation’ OR ‘disturbance’ OR ‘logging’ OR ‘grazed’ OR ‘livestock’. We compiled the articles for all years. In addition, we conducted a search in Google Scholar https://scholar.google.com (12 October 2024) using the keywords in English and Spanish. We ensured that the data collection effort was comprehensive, covering all community-scale mammal studies. The articles included in the analysis were only those in which the rate of visitation, number of seeds, viability or germination were informed for dispersers and/or dispersed plants.

2.2. Data Compilation

Each study was placed into one or more categories, depending on whether they reported the variables that make up the components of dispersal effectiveness. The categories recorded were visitation rate, number of faeces with seeds, number of seeds, seed viability, germination rate or percentage and number of seedlings, diet (plant species), landscape type (disturbed or undisturbed, and type of disturbance). The specific data reported by each article in the above categories were recorded, as well as the geographical locality (longitude, latitude, and altitude), the list of animal species, the year of publication and the journal in which the study was published. The most recent correct taxonomic identification of the animals and plants appearing in the reviewed articles was confirmed by consulting the Catalogue of Life, https://www.catalogueoflife.org/ (20 October 2024) (Table S1, Supplementary Materials).

3. Results

We compiled 275 studies from 52 countries, which were distributed as follows: South America (37.1%), Asia (25.4%), Europe (15.8%), North America (12.1%), Africa (7.7%), Central America and the Caribbean (1.1%), and Oceania (0.7%). Many of these studies were conducted in tropical and temperate forest biomes (Figure 1). The countries with the highest number of publications were Brazil (45), Argentina (23), Spain (22), the United States of America (17), Mexico (16), Japan (14), Chile, India and Thailand (11), and China and Colombia (10) (Figure 1A). The publication of these studies since 1990 has continued at a gradual pace (Figure 1B).

A total of 36.4% of the articles indicated that some form of disturbance was present in the study area. Of these, the only type of disturbance represented was anthropogenic. Only 5.8% of the articles analysed the effects of human disturbance on seed dispersal. The most common disturbances were logging (62.5%), agriculture (43.8%), livestock (31.3%), hunting (12.5%) and urbanization (12.5%). Many of these studies were conducted in Spain, Argentina, Brazil, China, Mexico, Kenya, Colombia, Indonesia and Cameroon.

The animals studied corresponded to 764 species belonging to 54 families, the most represented being Canidae (12.2%), Cervidae (6.4%), Sciuridae (6.3%), Mustelidae (6%), Phyllostomidae (5.8%) and Bovidae (5.2%). While articles addressing the effects of disturbance on dispersal detected a total of 52 species belonging to 22 mammal families, the most represented were Mustelidae (1.3%), Cercopithecidae (0.9%), Canidae (0.8%), and Sciuridae, Bovidae, Didelphidae and Viverridae (0.4%) (Figure 2A,B, Table S1).

The animals dispersed a total of 3618 plant species belonging to 199 families. The families with the highest number of species assessed were Poaceae (7.1%), Fabaceae (6.9%), Moraceae (6.2%), Rosaceae (5.8%) and Sapotaceae (2.8%). Only 8.1% of the articles reported whether the fruits consumed belong to native and/or introduced plant species. Studies addressing the effects of disturbance included a total of 112 plant species belonging to 47 families. Only 10 families were represented with more than one species: Fabaceae (0.4%), Rosaceae and Moraceae (0.3%), Arecaceae (0.2%), Poaceae, Cyperaceae, Annonaceae, Rubiaceae, Urticaceae and Anacardiaceae (0.1%) (Figure 2C,D, Table S1, Supplementary Materials).

Of the total 3618 plant species dispersed, 68.9% have fleshy fruits (drupe, berry, knob, aggregate fruits and fleshy capsules), while 30.02% have non-fleshy fruits (caryopsis, legumes, capsules and achenes), and in 1.08% of the cases it was not possible to determine the type of fruit. In the case of the plants that are present in the articles dealing with the effect of human disturbance on dispersal, the fruit types were distributed as follows: fleshy fruits (54.20%), non-fleshy fruits (43.51%), and unknown (2.29%) (Table S1, Supplementary Materials).

Many papers (78.9%) reported the number of seeds dispersed by animals, while 60% reported the rate of animal visits to plants. Of these, only 54.2% of the studies provided data on both variables. In 81.3% of articles that analysed the effect of disturbances, the number of visits was assessed. Additionally, 100% of these studies assessed the number of seeds dispersed per visit, while 75% assessed both the number of visits and the quantity of seeds dispersed (Figure 3).

Species of the family Canidae presented faeces with seeds of the families Rosaceae (3.9%) and Rhamnaceae (3.4%), among others. These data were obtained from research in North America (USA and Mexico), South America (Argentina), Europe (Spain), Asia (Japan) and Africa (South Africa). Species of the family Mustelidae mainly dispersed seeds of the family Rosaceae (2.2%) in Spain and China. Species of the family Sciuridae had the highest amount of faeces with seeds of the family Moraceae (1.1%) in Israel and Uganda. Research in Colombia, Mexico, Argentina and Peru mainly evaluated seed dispersal by the family Phyllostomidae, whose faeces contained mainly seeds of the Solanaceae family (2.8%).

Considering the quantity of seeds, the most frequent interactions were the following: Canidae–Rosaceae (3%), Canidae–Fabaceae (3%), Canidae–Rhamnaceae (3%), Mustelidae–Cornaceae (2.1%), Sciuridae–Moraceae (0.9%), Sciuridae–Rubiaceae (0.9%), Phyllostomidae–Solanaceae (2.6%) and Phyllostomidae–Moraceae (2.6%). These studies were mainly carried out in America (Argentina, Brazil, Costa Rica, Colombia, Peru, Bolivia, USA and Mexico), Europe (Spain and Hungary), Asia (Japan, India and Israel) and Africa (South Africa).

A total of 49.1% of the articles referred only to the proportion of viable seeds, 69.1% to the proportion of germinated seeds and established seedlings, and 49.5% to both variables. Of the studies that analysed the effects of anthropogenic disturbances, 81.3% assessed the proportion of germinated seeds and established seedlings and the proportion of viable seeds (Figure 4).

Regarding seed viability after fruit ingestion, Canidae species consumed fruits of Rosaceae (4.7%), Fabaceae (4.0%) and Rhamnaceae (3.4%) plants in Argentina, Bolivia, USA, Mexico, Spain, Japan and South Africa. While Mustelidae species consumed fruits of the Rosaceae family in Spain and China, Cervidae species consumed fruits of Caryophyllaceae in Norway and Switzerland, and Phyllostomidae species consumed fruits of Solanaceae in Colombia, Argentina, Mexico and Peru.

The effect of passage through the digestive tract on seed germination was evaluated in seeds of the families Rosaceae (3.9%) and Rhamnaceae (3.4%), consumed by species of the family Canidae, in studies carried out in Argentina, Mexico, USA, Spain, Japan and South Africa. In the case of Mustelidae, germination was evaluated in seeds of Rosaceae (2.4%) and Ericaceae (2.4%), in Italy, Portugal, Spain, USA and China. For the family Phyllostomidae, the analysis was carried out on seeds of the family Solanaceae (2.4%) in Mexico, Colombia, Argentina and Peru.

In 48.4% of the scientific articles reviewed, the authors simultaneously assessed the quantity and quality of dispersal, although only 12 of them (4.4%) calculated the SDE. None of the articles that addressed the effectiveness of seed dispersal by mammals analysed the effects of human disturbance on this process (Figure 5).

In the studies reviewed, the highest percentages of articles analysed the following combinations of variables: Number of seeds + Germination (60.4%), Number of visits + Germination (50.5%), and Number of visits + Number of seeds + Germination (50.2%). Twelve studies addressed the components of effectiveness associated with the effects of anthropogenic disturbances, with the combinations Number of seeds + Germination (93.8%), Number of seeds + Viability and Number of seeds + Viability + Germination (81.3%) being the best represented.

There was a positive effect of human-mediated disturbance in six studies. In three of them it was negative, and in seven of them the number of visits was not analysed. Eight studies reported a positive effect on the number of seeds, while seven reported a negative effect, and in one study this was not analysed. The effect of disturbances was positive for the seed germination process in two of the studies that were addressed in the analysis, and seed viability was not analysed in any of the articles reviewed (

Table 1. Direction of the effect of anthropogenic disturbances on the subcomponents of seed dispersal effectiveness addressed in the reviewed scientific literature.

Disturbance	Country	Frugivore	Plant	Quantity Component		Quality Component		Reference
				Number of Visits	Quantity of Seeds	Viability	Germination
Agriculture and urban expansion	Spain	Vulpes vulpes Martes foina Meles meles Genetta genetta Sus scrofa	Ziziphus lotus	NA	Negative	NA	NA	Cancio et al. (2016) [60]
Hunting and logging	Colombia	Dasypus novemcinctus Tayassu pecari Priodontes maximus Eira barbara Didelphis marsupialis Nasua nasua Dasyprocta fuliginosa Leopardus pardalis Proechimys sp. Marmosa robinsoni Dasyprocta punctata Microsciurus mimulus Sciurus granatensis	Oenocarpus bataua	Negative	NA	NA	NA	Franco-Quimbay and Rojas-Robles (2014) [61]
Logging, livestock and agriculture	México	Alouatta palliata mexicana	Ficus perforata Ficus lundelli	NA	Positive	NA	Positive	Serio-Silva and Rico-Gray (2002) [62]
Livestock	Argentina	Microcavia australis Lycalopex griseus Graomys griseoflavus Akodon dolores Conepatus chinga Chaetophractus vellerosus Calomys musculinus Galictis cuja Leopardus geoffroyi Thylamys pallidior Dolichotis patagonum	Neltuma flexuosa	Positive	Positive	NA	NA	Miguel et al. (2018) [63]
Logging	Indonesia	Viverra tangalunga	Adenia sp. Alangium sp. Annona sp. Connarus sp. Dialium indium Dimocarpus longan Ficus sp. Garcinia sp. Glochidion sp. Microcos sp. Palaquium sp. Polyalthia sp. Pometia pinnata Psidium sp.	NA	Negative	NA	NA	Colon and Sugau (2012) [64]
Urban expansion, agriculture and livestock	México	Ateles geoffroyi	Spondias radlkoferi Spondias mombin Attalea butyracea Bactris balanoidea Sabal mexicana Sapium sp. Acacia farnesiana Dialium guianense Inga punctata Inga sp. Calatola laevigata Nectandra sp. Guarea glabra Guarea grandifoliola Brosimum alicastrum Castilla elastica Ficus sp. Ficus tecolutensis Ficus obtusifolia Faramea occidentalis Paullinia costata Ampelocera hottlei Celtis iguanaea Cissus verticillata	NA	Negative	NA	NA	Chaves et al. (2010) [65]
Logging and agriculture		Lycalopex gymnocercus Pecari tajacu	Acacia aroma Acacia gilliesii Bromelia urbaniana Cactaceae Celtis ehrenbergiana Cucurbitella asperata Geoffroea decorticans Prosopis flexuosa Prosopis torquata Ziziphus mistol	Negative	Negative	NA	NA	Periago et al. (2017) [66]
Logging	China	Melogale moschata	Dendrobenthamia japonica Dendrobenthamia capitata Clematoclethra scandens Actinidia chinensis Diospyros lotus Hovenia dulcis Prunus salicina	NA	Negative	NA	NA	Zhou et al. (2008) [67]
Agriculture and logging	Kenya	Cercopithecus mitis Cercopithecus ascanius Colobus guereza	Prunus africana	Positive	Positive	NA	NA	Farwig et al. (2006) [68]
Logging and hunting	Brazil	Dasyprocta leporina	Astrocaryum aculeatissimum	Negative	Negative	NA	NA	Galetti et al. (2006) [36]
Livestock and agriculture	Spain	Canis lupus Genetta genetta Martes foina Martes martes Meles meles Mustela erminea Mustela nivalis Ursus arctos Vulpes vulpes	Crataegus monogyna Ficus carica Frangula alnus Malus domestica Prunus avium Prunus domestica Prunus spinosa Pyrus communis Pyrus cordata Rosa spp. Rubus spp. Sorbus aucuparia Vaccinum myrtillus Vitis vinifera	NA	Positive	NA	NA	López-Bao and González-Varo (2011) [40]
Agriculture	Spain	Rodentia	Quercus ilex	NA	Negative	NA	NA	Morán-López et al. (2016) [20]
Livestock and logging	Argentina	Dolichotis patagonum Lycalopex griseus	Neltuma flexuosa	Positive	Positive	NA	NA	Miguel et al. (2017) [19]
Logging	China	Apodemus peninsulae Apodemus draco Sciurotamias davidianus	Quercus aliena var. acuteserrata	Positive	Positive	NA	NA	Yu et al. (2017) [69]
Experimental burns	Brazil	Tapirus terrestris	Bellucia grossularioides Byrsonima crispa Enterolobium schomburgkii Eriotheca globosa Glycine max Guatteria schomburgkiana Humiria balsamifera Hymenaea courbaril Mauritia flexuosa Passiflora sp. Protium guianense Ricinus communis Sacoglottis guianensis Schefflera morototoni Senna sp. Solanum sp. Strychnos xinguensis Terminalia tetraphylla	Positive	Positive	NA	NA	Paolucci et al. (2019) [70]
Logging	Cameroon	Cephalophus natalensis Cephalophus silvicultor Philantomba congica	Ageratum conyzoides Axonopus compressus Cardamine sp. Cyperus sp. Ficus sp. Ficus wildemaniana Fimbristylis sp. Kyllinga sp. Laportea aestuans Mitracarpus hirtus Musanga cecropioides Oplismenus burmannii Oxalis barrelieri Oxalis sp. Panicum laxum Paspalum conjugatum Phyllanthus sp. Torenia thouarsii	Positive	Positive	NA	Positive	Houngbégnon et al. (2023) [71]

NA = variable not assessed.

).

4. Discussion

The study of frugivory and seed dispersal by mammals has been conducted across all continents, with South America representing the most extensively researched region. This knowledge has been accumulated over the last 30 years, during which time it has become clear that many species of mammals and plants are involved in this interaction. However, these investigations have been focused more often on the quantity of seeds dispersed, rather than the quality of dispersal. Regarding the quantity of seeds dispersed, their assessment in faeces has been the subject of less study than the number of visits to plants. Considering the quality of dispersal, seed germination has been the subject of more extensive study than seed viability. Moreover, the number of studies that assess the effectiveness of seed dispersal by mammals, considering both the quantity and quality of dispersal, is very low. Unfortunately, there is still a paucity of studies assessing the impact of human activities on the effectiveness of seed dispersal by mammals.

Many of the studies reviewed focus on South America, Asia, Europe and North America. This does not reflect the wide and diverse geographical distribution of mammals, which can be found in all biomes across the globe. The limited research in areas where mammals are present may be due to a lack of financial resources, a shortage of researchers, or a lack of interest in this subject. It is, therefore, evident that further research is required on the subject of seed dispersal by mammals, given that they play an important role in this process in all terrestrial ecosystems around the world where they have been evaluated [72,73,74,75,76,77]. Currently, there are numerous literature reviews and/or meta-analyses on frugivory and seed dispersal by mammals and the effect of disturbance on this process [21,34,78,79,80,81,82,83,84,85,86,87,88]. Unfortunately, only few studies have analysed the effectiveness of seed dispersal and how the components have been affected by anthropogenic disturbance.

The primary seed-dispersing families are Canidae, Mustelidae and Cervidae. Carnivores have traits that make them important frugivores and seed dispersers, which sets them apart from birds and other frugivorous mammals. It is worth noting that mammals are not typically migratory animals like birds. Most of them can consume fruits year-round, rather than just during a specific season. Furthermore, carnivores are opportunistic foragers, adapting their diet according to prey availability. This results in increased fruit consumption during periods of greater environmental supply [67,88,89,90]. Bats are recognised as one of the most significant frugivorous vertebrates in the Neotropics, playing an invaluable role in seed dispersal [72,91,92,93]. One aspect of the feeding behaviour of bats is that they carry fruits to their feeding roosts before consuming them. This enables most of the seeds handled by fruit bats to be carried away from the vicinity of the mother plant, as they are volant species. This benefits their seed dispersal process. Primates represent another significant group of seed-dispersing frugivores, with neotropical species representing the most extensively studied category [81,82,94,95,96,97,98]. An exception is the Pithecines, which have developed highly specialised dental and gastrointestinal adaptations enabling them to eat and feed on seed contents. This has defined them as seed predators (granivores) [99]. Unfortunately, that there are still considerable gaps in our knowledge of primates in Asia and Africa regarding frugivory and seed dispersal. It is often assumed that ungulates are seed predators due to their powerful digestive system, which enables them to process seeds effectively through fine chewing and efficient microbial digestion [100]. It should be noted, however, that these animals play a mutualistic role as seed dispersers [12,101,102].

There is a high level of diversity in plant species dispersed by mammals, with the majority belonging to the families Poaceae, Fabaceae and Rosaceae [54,74,98,103,104]. The fruits of these latter two families are drupes, berries and fleshy arils, which are consumed by carnivores, primates, New World marsupials and elephants. These animals are attracted by the pulp, which is rich in sugars and minerals. The families Poaceae and Fabaceae produce dry fruits of the caryopses and legume types, respectively. These are consumed by ungulates as part of their diets. However, forest species of trees and shrubs are less resistant to intestinal transit by ungulates than open field species. It is worth noting that tree seeds are often too large to survive the chewing process and intestinal transit, and are produced in too low quantities, which reduces the effectiveness of dispersal by ungulates. The results of this study indicate that carnivores consume a significant number of pomes, drupes, berries, arils, and dry cones. The families Rosaceae, Moraceae, and Ericaceae stand out as the most prevalent in this regard. The consumption of this variety of fruits is due to the fact that this zoological lineage does not present morphological restrictions, in contrast to small-sized birds. Therefore, carnivores can consume infructescences of small fruits such as those of Sorbus aucuparia, whole fruits such as those of Pyrus bourgaeana and Chamaerops humilis [54,105], and pieces of fruits when these are large, such as pears Pyrus communis and apples Malus domestica [40] or have an irregular shape such as those of Hovenia dulcis [106]. Canids are frequently observed consuming legumes belonging to the Prosopis genus (Fabaceae). This behaviour has been shown to act as an effective means of seed dispersal [107,108,109,110,111,112,113,114]. Primates also consume the fruits of these plant families, which are eaten by both ungulates and carnivores. This results in the effective dispersal of seeds [81]. For example, primates play an important role in the dispersal of Virola flexuosa seeds. Therefore, a decline in these animals could potentially limit the dispersal of this plant. The genetic flow of seedlings of the tree Inga ingoides in forest areas where the spider monkey (Ateles paniscus) is present is greater than in areas where this primate has been extirpated. Similarly, the density of seedlings of the tree Dialium guianense is higher in forest patches inhabited by the howler monkey (Alouatta palliata) than in patches not occupied by this primate [115]. This demonstrates that the diet of seed-dispersing frugivorous mammals is varied, including fruits of different types belonging to plant species from several families.

A significant body of research has been conducted on the topic of dispersed seeds, with studies focusing on two key areas: the number of visits and the number of seeds found in faeces. In terms of the number of visits, different methodologies are used to obtain this information. These include the analysis of the amount of faeces with seeds [54,74,75,77,116], seed removal experiments [117,118,119,120], the use of camera traps [117,121,122,123] and direct observation [68,118]. The application of these techniques enables the degree of frugivory exhibited by animals to be determined, which varies between species. This can be categorised as either highly frugivorous or incidental frugivorous, with implications for the effectiveness of seed dispersal [12]. Carnivores are more likely to visit plants from which they can consume fruits when herbivores and frugivores improve access to these plants. This can be achieved by removing thorny vegetative parts or knocking the fruits off the plants. These opportunistic frugivores mainly consume the fruits that fall to the ground. The presence of predators has an impact on the visitation rate. For instance, the consumption of Pyrus bourgaeana fruits by Vulpes vulpes, Meles meles and Martes foina is reduced in areas where the Lynx pardinus is present [121]. To determine the quantity of seeds dispersed, two main approaches are typically employed: the estimation of the number of seeds present in faeces [52,74,111,124,125,126,127], and the calculation of the frequency of seed occurrence [113,128,129,130,131,132]. It is established that the manner in which carnivores process the fruits they consume results in minimal processing [133]. As a result, carnivores consume a significant quantity of fruits and defecate the seeds without causing much damage by chewing [41,134]. In contrast, primates handle fruits with precision and occasionally spit out seeds, as well as employing another dispersion method through regurgitation [82,97]. In the case of ungulates and lagomorphs, which have molars that can effectively process the majority of seeds ingested, the quantity of these seeds present in the faeces is significantly reduced [41,51,54,135]. To illustrate this, the seeds of Crataegus monogyna are conumed by a variety of mammals, including the wild boar (Sus scrofa) which destroys 90% of the seeds it ingests [135]. The analysis of the number of seeds in faeces allows the effectiveness of animals in seed dispersal to be determined [136], because the ability of the animals to carry seeds to safe sites is evaluated, without determining their survival and germination. This also allows the degree of frugivory and effectiveness to be determined [12,13].

The quality of seed dispersal is evaluated through the analysis of seed viability and germination rates, as well as the recruitment of seedlings [12,13]. The application of these subcomponents in research is uneven, with the analysis and comparison of seed germination being the predominant approach. It is important to consider the handling of fruits and seeds by animals, given the treatment these undergo in the mouth and digestive system [75,103,137,138,139]. It has been suggested that the digestive process does not have a negative impact on seed viability, particularly in the case of fleshy fruits [140]. This is in contrast to nuts and dried fruits, which have the highest percentage of non-viable seeds due to their tendency to break down [88]. It is, therefore, our conclusion that the ingestion and subsequent digestion of fruits consumed by carnivores has a neutral effect on seed viability [126,141]. Conversely, germination has been extensively researched, with a particular focus on the impact of animal digestion on seed germination speed and/or capacity [78,142,143]. The consumption of fruits by mammals has a generally positive effect on seed germination. In some cases, it increases the number of seeds that germinate, while in others, it accelerates the germination process. It should be noted, however, that this effect is not universal across all mammal species [78]. In the case of the nectarivorous and frugivorous bat Leptonycteris yerbabuenae, the germination of seeds is found to decrease after ingestion. There are two possible explanations for this phenomenon. Firstly, the acids in the gastrointestinal tract of these animals may kill the embryos that are inside the seeds [144]. Secondly, the digestive system of this bat is simple, and the digestion of fruits is less efficient than in other bats [145]. It is worth noting that only members of the Ursidae family significantly increase seed germination, in contrast to species from the Viverridae, Canidae, Mustelidae and Procyonidae families, which have mostly neutral effects [78]. This may be due to the fact that these carnivores have short gastrointestinal systems, which limits the interaction time with seeds and, consequently, reduces the scarification process, i.e., breaking of the layers that surround the embryos found inside the seeds, whether mechanically or biochemically [146]. It has been demonstrated that in primates, there are differences in the effects on germination depending on the food group [82]. Strictly frugivorous primates typically enhance seed germination by 75% in comparison to uneaten seeds [81]. This is linked to the fact that species in this category tend to have a larger body size and consume fruits with relatively large seeds, which benefit from the passage through the gastrointestinal tract [82]. It was found that other feeding guilds of Neotropical primates provided a less reliable dispersal service. The folivores–frugivores, who rely more on leaves in their diet but also eat a large amount of fruit, were the second-best feeding guild in terms of increasing germination [81,82,97]. In contrast, primates that include a significant fraction of insects in their diet, such as frugivores–insectivores and insectivores–frugivores, did not significantly affect the percentage of seed germination, but in fact, delayed the germination process [81,82,97]. The analysis of viability and germination according to animal and plant families indicates that phylogeny may be a significant factor in determining the quality of seed dispersal [119,127,137,147,148]. Therefore, it is essential to evaluate both subcomponents in future studies and to complement them with an analysis of the effects that the treatment has on mastication and digestion of seeds of native or exotic species by native or introduced animals.

There is a paucity of studies that evaluate the effectiveness of seed dispersal. Only two articles (1.5%) analyse quantity and quality without calculating effectiveness, and only one (0.8%) does so. To illustrate, the Andean bear (Tremarctos ornatus) in the Apolobamba region of Bolivia plays a crucial role in the dispersal of plants. Furthermore, the seeds of Nectandra cf. cuneatocordata, Symplocos cf. cernua and Gaultheria vaccinioides remain unharmed and viable after being ingested [149]. In contrast, the pampas fox (Lycalopex gymnocercus) in the mountains of Córdoba, Argentina, disperses significant quantities of Pyracantha atalantoides seeds, which germinate successfully after being consumed by the fox [103]. Finally, another study addressed the effectiveness of seed dispersal by calculating the SDE and compared the quantitative and qualitative contributions between birds and mammals [150]. The study examined the complementarity of seed dispersal services provided by the blueberry Vaccinium myrtillus in an alpine ecosystem in Poland. It focused on the role of capercaillies, passerines (birds] and carnivores, including Ursus arctos, Vulpes vulpes and Martes sp. The evaluation of the differences in quantity and quality of seed dispersal revealed that both bird and mammal species are effective dispersers of blueberries. This may be because the arrival of seeds to different microhabitats suitable for germination is guaranteed, which maximises the chances of seedling recruitment [150]. The development of studies that evaluate the effectiveness of seed dispersal presents certain challenges, including the need to evaluate all variables, which is not always feasible due to material, economic, or time constraints. However, further development is required to gain a deeper understanding of the significance of seed dispersal effectiveness in the context of plant–animal interactions, both from an ecological and an evolutionary perspective.

Only 6% of the studies incorporated human disturbance variables into their analyses. It was anticipated that there would be a reduction in the visitation rates in areas affected by anthropogenic disturbances. However, only one study indicated that an anthropogenic disturbance had a negative impact on the visitation rate, while six studies indicated positive effects. The study with negative effects revealed that rodents that disperse the seeds of the species Quercus aliena var. acuteserrata in exotic plantation stands in China exhibit the lowest rates of visitation in logged areas. This is due to the fact that the abundance of these dispersing mammals is reduced in these habitats, as they are more easily detected by predators [69]. A reduction in seed quality was anticipated in disturbed areas. However, this was not found in many of the reviewed studies, with six reporting positive effects and only two identifying negative impacts. One of the latter studies addressed the dispersal of seeds of the palm Astrocaryum aculeatissimum by the agouti (Dasyprocta leporine), its main disperser [36]. They found the frugivory and seed dispersal processes were collapsing as a result of a reduction in the quantity of seeds dispersed in areas where these animals have been extirpated [36]. Our expectation was that there would be no net effect on seed viability, given that this is largely dependent on the physiological characteristics of the animals involved, rather than on the characteristics of the environment. Unfortunately, we were unable to identify any studies that had evaluated this aspect. Finally, regarding germination, we anticipated a negative impact resulting from alterations in the structure of habitats affected by human disturbances. Unfortunately, this was only studied in a single investigation, which reported a positive effect [71]. As a result, it is not possible to obtain general conclusions in this regard. The study assessed the role of three species of African antelopes, Cephalophus natalensis, Cephalophus silvicultor and Philantomba congica, in seed dispersal in logged and unlogged areas. This was the first documented instance of viable seeds belonging to tropical forest species germinating in logged areas, underscoring their significant ecological contribution to forest regeneration [71].

5. Conclusions

This review has identified two main areas where further research would be beneficial. Firstly, there is a lack of studies addressing the calculation and analysis of the effectiveness of seed dispersal. Secondly, there is a lack of studies analysing the effects of landscape disturbance on seed dispersal by mammals. Bridging these gaps in knowledge would be valuable, as it would help us to understand the plant–mammal interaction in the context of the current global scenario, where natural habitats are being altered and lost, affecting the regeneration of plant species.

It is important to continue analysing seed dispersal patterns by mammals in areas affected by logging, hunting, and land use change [agriculture and livestock], as well as other types of anthropogenic disturbances such as mining and urbanization. Such analyses may reveal key behavioural mechanisms underlying changes in dispersal effectiveness, detect possible causes of dispersal failures, and improve management practices to increase natural forest recovery.

To achieve conservation goals related to plant–frugivore mutualist relationships, it is recommended that corridors be created to enable the movement of dispersers between fragmented areas [151,152]. It is also recommended that plants that play an important role in the interaction networks be included in reforestation plans [153]. With regard to the presence of roads in forested areas, it would be beneficial to maintain or increase the density of woody vegetation along roadways in order to mitigate the impact of fragmentation on seed dispersal [28]. To develop effective strategies for the protection of frugivores, it is necessary to reduce hunting. This can be achieved by providing economic incentives to human populations living close to the distribution areas of these species [154]. Another option is the reintroduction of functional dispersers or fruit-eaters that have become locally or globally extinct [155]. A reduction in logging, coupled with the reforestation of affected areas with native plant species, can also help to offset the impact of this disturbance on seed dispersal. The findings of research on invasive plant dispersal will facilitate the modelling, prediction and prevention of invasions, enabling the development of more effective eradication strategies for both invasive plant and animal species using seed dispersal cores [156]. These recommendations will reduce the effects of human disturbance on the seed dispersal process of mammals by conserving and restoring populations of dispersers and dispersed plants.