Perspective Chapter: The Antioxidant and Other Biological Roles of Different Species of Seaweed in Enhancing Poultry Growth and Health

Fisayo Oretomiloye; Deborah Adewole

doi:10.5772/intechopen.1011791

Abstract

Seaweeds are bioactive substances that are excellent sources of antioxidants, carbohydrates, protein, vitamins, and minerals. The role of seaweeds in animal nutrition is all-encompassing, some of which includes boosting growth performance; enhancing meat and egg quality, immune status; and preventing inflammation, oxidative stress, and microbial infections. In poultry, the efficacy of different seaweed species in improving growth performance and immune and antioxidant status has been established in many studies. The major concerns associated with the effectiveness of seaweed are the dosage level, ash content, and anti-nutritional factors. Inconsistencies in the outcomes might be directly linked to specific bioactive substances in different seaweed species. This review aims to identify different species of seaweed, their contents of bioactive substances, their unique roles, and the possible mechanisms of action with respect to growth performance, immune health, and antimicrobial and antioxidant capacity.

Keywords

antioxidants
bioactive compounds
immune health
poultry
seaweed

Author Information

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Fisayo Oretomiloye
- Lethbridge Research and Development Centre, Lethbridge, Canada
Deborah Adewole *
- Department of Animal and Poultry Science, College of Agriculture and Bioresources, University of Saskatchewan, Saskatoon, Canada

*Address all correspondence to: deborah.adewole@usask.ca

1. Introduction

The poultry industry is fast-growing and expected to expand as consumer demands increase due to its low cost and rich nutritional profile [1]. Poultry has contributed significantly to global food security and the economy [2]. Globally, poultry meat is anticipated to account for 41% of all sources of meat-based protein in 2030 [3]. According to Agriculture and Agri-Food Canada, Canadian farmers produced 1.30 billion kg of chicken, generating $3.3 billion and contributing 4% to farming operations, in 2021 [4]. The overall chicken meat consumption in Canada has tripled in recent years, partly due to the continuous rise in the population from 24.5 million in 1980 to over 38.7 million in 2022, accounting for an almost 58% increase [5]. The rising consumption trend of chicken reflects the general acceptability and affordability across all regions. Antibiotics have undoubtedly contributed to increased chicken production; however, antibiotic usage is winding down in poultry production due to resistance issues [6]. Focus has shifted to developing feed supplements that can enhance poultry performance and food safety benefits [6]. Alternative feed supplements, such as plant extracts, probiotics, prebiotics, symbiotics, enzymes, and organic acids, have been extensively studied [7, 8, 9, 10] for their biological activity. These feed supplements have been well documented to boost growth performance, reduce pathogenic bacteria population, and enhance gut health and immune functions [11, 12, 13, 14, 15].

Seaweeds have been utilized as alternative feed ingredients for animals in recent years because of their numerous health benefits [16], nutritional contents, pigments, antioxidant and prebiotic activities [17], availability, and low cost [18]. Seaweeds (marine macroalgae) are a diverse and widespread group of photosynthetic organisms found in almost all aquatic environments, marine and freshwater, and from tropical islands near the equator to polar regions [19]. Taxonomically, seaweeds are classified as Chlorophyta (green seaweed), Phaeophyta (brown), and Rhodophyta (red) based on their pigment composition [17, 20]. The green coloration is due to the presence of chlorophyll a and b; the brown algae color is due to xanthophyll pigment and fucoxanthin; while the red algae color is due to phycoerythrin and phycocyanin [21]. At the ecological level, macroalgae function as essential primary producers and habitat-structuring organisms that support food production, nutrient cycling, energy flow, and coastal defense [22]. Seaweeds used in animal feeding can be either wild-harvested or cultivated. Wild-harvested seaweeds are harvested from natural coastal ecosystems [23] and result in multiple mixed species, high variability in nutrient composition, and contamination from the surrounding environment [24]. On the other hand, cultivated seaweeds are known as seaweed aquaculture and are grown under a controlled system [25] that allows for improved safety and sustainability. Global seaweed production (wild-harvested and cultivated) increased over 60 times, from 0.56 million (wet) tons in 1950 to 35.82 million tons in 2019. This growth has been driven mostly by aquaculture, with cultivated algae accounting for 34.74 million tons in 2019, while only 1.08 million tons were harvested from the wild [26]. The rise in cultivated seaweed production is connected to the farming of brown, red, and green seaweeds, with distinct species and cultivation practices dominating in different countries. In 2019, the Laminaria/Saccharina japonica was mainly cultivated in Eastern Asia and Europe [27]. Red seaweed cultivation is generally found in Asia, Eastern Africa, Pacific Island states, Latin America, and the Caribbean. The green seaweeds are rarely grown commercially and primarily comprise five species: Capsosiphon fulvescens, Caulerpa spp., Monostroma nitidum, Enteromorpha (Ulva) prolifera, and Codium fragile [27], with Ulva being the most dominant genus [28]. The cultivation of brown seaweeds increased from 13,000 tons in 1950 to 16.4 million tons in 2019 worldwide, where it accounted for 47.3% of world seaweed cultivation in terms of tonnage and 52% in terms of value, while red seaweeds accounted for 52.6% of global seaweed cultivation [27]. Beyond their economic value, seaweeds are known for their excellent nutritional profiles, which vary across different groups and species. For example, red seaweed is highly digestible due to its fiber content than brown and green seaweed. Red seaweeds possess quality fatty acids essential to human health, while green seaweeds are generally high in minerals and vitamins, and brown algae are rich in vitamins E and C [29, 30]. Table 1 shows the nutritional composition of common seaweed species for poultry nutrition. Seaweed health benefits are associated with their nutritional composition, including minerals, vitamins, phlorotannins, alginate, diterpenes, and sulfated polysaccharides [29]. Different forms of seaweed—naturally occurring, cultivated, or their extracts—may be applied in poultry feeds and can improve poultry health and performance [18]. The use of seaweed in animal feeds accounted for the second-largest seaweed market in 2017 and is projected to increase due to current research impacts focusing on improved animal health and productivity [31].

Parameter	Ulva spp. (Green)	Chondrus crispus (Red)	Palmaria palmata (Red)	Laminaria spp. (Brown)	Ascophyllum nodosum (Brown)
Crude protein, %	13.3–23.1	9.8–12.5	18.48	0.6–20.5	5.6–12.1
Crude Fiber, %	12.31	3.1–4.5	1.83–3.5	13.3	4.1–6.8
Crude fat, %	0.1–6.6	0.7–1.7	1.2–1.3	0.5–1.3	2.9–5.8
Ash, %	12.9–54.4	21	12–37	14.2–38	18–29.5
Carbohydrate, %	36–58	55–68	46–56	48	59.1–62.8
Calcium, %	0.524–6.15	0.420–1.120	0.12–1.200	1.005	0.98–3.41
Phosphorus, %	0.14–0.21	0.135	0.235–0.33	0.12–0.3	0.05–0.23
Sodium, %	1.595–2.93	1.200–4.270	1.600–2.500	3.818	2.73–5.2
Potassium, %	1.51–1.561	1.350–3.184	7.000–9.000	0.0115–0.079	1.4–8.7
Magnesium, %	1.90–2.094	0.600–0.732	0.170–0.610	0.659	0.57–1.14
Copper, mg/kg	3.4–146.8	<5.0	1.24	1.0–20.0	1.6–17
Iron, mg/kg	139–5800	39.7	35.51	11.9–702	100–370
Manganese, mg/kg	11.0–637	13.2	7.62	2.9–38	10–56.8
Zinc, mg/kg	6.0–63.8	71.4	7.24	1.0–81.0	28–114

Table 1.

Nutritional composition of common seaweed species for poultry nutrition.

Nutritional composition of the main seaweed species used as animal feed (all values are ranges based on several studies and are expressed on a dry weight basis). Values are compiled from Ulva spp. [29, 32, 33, 34], Chondrus crispus [29, 35, 36, 37], Palmaria palmata [29, 35, 36, 38], Laminaria spp. [29, 32, 39], and Ascophyllum nodosum [32, 34, 36].

2. Seaweed bioactive compositions and bioactivity

Seaweeds are rich in bioactive compounds and are utilized as functional ingredients in animal health applications. Bioactive substances, including sulfated polysaccharides, phlorotannins, and fucoxanthin from marine algae, are known to exert biological activities such as anticoagulant, antioxidant, antiviral, and antitumor activities [40, 41, 42]. Phlorotannins, a class of phenolic compounds in brown seaweed, are produced through the polymerization of phloroglucinol, and these compounds have varying molecular weights ranging from 126 to 650 kDa [43]. The major classes of phlorotannins have been previously listed as fucols, fuhalols, fucophlorethols, phlorethols, carmalols, and eckols [44]. Considering in vivo and in vitro studies, no significant effect was observed on the effect of 0.2% phlorotannin extract from brown seaweed on Campylobacter colonization and growth performance of chickens [45]. Phlorotannin can prevent the growth of bacteria by destroying the cell membrane, DNA, and protein [46]. Further studies should investigate the bioavailability of phlorotannins in poultry health. Brown seaweeds produce diverse polysaccharides, such as fucoidans, laminarans, and alginates. Laminarans and fucoidans are the major water-soluble polysaccharides of brown seaweeds, while alginic acids are alkali-soluble polysaccharides and possess high molecular mass [21, 47]. Fucoidan has received much interest because its unique biological actions bestow nutritional and health benefits on humans and animals. The biological activities of fucoidans are associated with their structure and chemical composition, which can be affected by the extraction process, geographical location, and harvest season [48]. An in vitro model suggested that high molecular weight fucoidan from Fucus vesiculosus could be an effective radical scavenging agent and could be related to its molecular weight, sulfate, and polyphenol contents [49]. An in vitro study found that fucoidan from brown seaweed and the sulfated galactan from red seaweed had higher antioxidant capacity than commercial carrageenans through the oxygen radical absorbance capacity method [50]. Meanwhile, no correlation was found between sulfate content and antioxidant capacity [50]. The sulfate content of a sulfated polysaccharide is one of the determining factors for its biological activity. The sulfate contents of the polysaccharide fractions isolated from Sargassum pallidum showed a high correlation between low molecular weight and the highest sulfate content [40]. Rocha De Souza et al. found a positive relationship between sulfate content and antioxidant activity and indicated that fucoidan from brown seaweed and lambda carrageenan from red seaweed demonstrated the most excellent free radical scavenging potential and antioxidant ability compared to other polysaccharides (iota, kappa carrageenan, fucans) [51]. Another study found that the scavenging activity of sulfated polysaccharides from red seaweed (Gracilaria birdiae) increased significantly for higher polysaccharide concentrations, which affirmed that sulfate content had a significant effect on the antioxidant activity [52]. Comparing the antioxidant activity of polysaccharides from different seaweeds, fucoidan from Lessonia vadosa and sulfated galactan from Schizymenia binderi exhibited higher antioxidant capacity than commercial carrageenans using the oxygen radical absorbance capacity method [50].

Fucoxanthin is one of the most dominant carotenoids from brown seaweed. It has a small molecular weight and can protect cell components from oxidative damage [53]. Fucoxanthin has been reviewed for its diverse biological activities, such as antioxidant, anti-inflammatory, and neuroprotective functions [54]. Fucoxanthin previously improved the appearance and shelf life of chicken products [55]. Other antioxidant activities of fucoxanthin extract have been described in the previous section. Red seaweeds also contain great amounts of polysaccharides, particularly within the cell wall matrix, which are quite different from terrestrial medicinal plants. Red seaweed polysaccharides possess excellent biological activity and are mainly made up of carbohydrates [56]. The total polyphenol content of red seaweed has been previously reviewed, and the values varied between 25.8 and 5121 mg GAE/100g, with a median value of 127mgGAE/100 g, which is lower than those found in brown algae [30]. The polyphenols found in red seaweed are protocatechin, hydroxybenzoic acid, and bromophenols, which are different from brown algae polyphenols [30]. Figure 1 summarizes the bioactive composition of different types of seaweed.

Figure 1.
Summary of the bioactive composition of specific types of seaweed.

3. Biological roles of different species of seaweed

Different species of seaweeds, including brown, red, and green, have been studied for their biological activity in poultry. The antioxidant modes of action and other biological roles of seaweed, including growth performance, immune health, and antimicrobial properties, are further discussed in this review. Figure 2 summarizes seaweed’s major bioactive compounds and their mechanisms of action.

Figure 2.
Seaweed major bioactive compounds and their mechanisms of action. Abbreviation: SW, seaweed; T-AOC, Total antioxidant capacity; GS, Glutathione reductase; GPX, Glutathione peroxidase; CAT, catalase; SOD, Superoxide dismutase; MDA, Malondialdehyde; FCR, Feed conversion ratio; FI, Feed Intake; ABWG, Average body weight gain; IgA, Immunoglobulins A; IgM, Immunoglobulins M; IgG, Immunoglobulins G; VH, Villus height; VW, Villus weight; CD, Crypt depth.

3.1 Antioxidant modes of action of seaweed

Seaweed has been proven to possess a strong antioxidant capacity that can maintain balanced redox status in poultry birds [57, 58]. Seaweed polysaccharides combat oxidative stress by modulating apoptotic-related signaling pathways to repair the damage triggered by oxidative stress [59]. Diverse studies have investigated the antioxidant activity of Enteromorpha prolifera, a type of green seaweed that is abundant in Asia, which is known for its excellent antioxidant capacity [60]. Dietary supplementation of Enteromorpha powder increased the glutathione peroxidase activity in the serum and ovary tissues and reduced malondialdehyde levels in the liver and ovary tissues in Zi geese [58]. Polysaccharides from Enteromorpha spp. enhanced the serum catalase and liver superoxide dismutase activities (d 21 and 35), the serum glutathione peroxidase (d 35), and decreased malondialdehyde in serum, liver, duodenum, and jejunum on d 21 and 35 [57]. The polysaccharides are water-soluble sulfated polysaccharides and were extracted from Enteromorpha using enzymatic methods, purification, and spray drying [57]. Further analysis suggested that the strong antioxidant activity of the extracts from Enteromorpha prolifera was because of a chlorophyll compound, pheophorbide a, rather than phenolic compounds [60]. Among the four studied green seaweeds [61], Enteromorpha compressa and Capsosiphon fulvescens were the most efficient hydroxyl scavengers and demonstrated the strongest antioxidant potency compared to Chaetomorpha moniligera and Ulva pertusa. The antioxidant properties correlate with flavonoid content rather than the total phenolic content [61]. The green algae, Ulva rigida, had a higher total phenolic compound of 73 mg gallic acid 100 g⁻¹ FW than several seaweeds [62]. Differences in the amount of phenolic compounds have also been confirmed in brown seaweeds. Mhadhebi et al. observed differences in the phenolic composition of three brown seaweeds: Cystoseira crinite, Cystoseira sedoides, and Cystoseira compressa, in which Cystoseira compressa exhibited the highest total phenolic content [63]. High total phenolic content correlates with excellent radical scavenging activity [64, 65]. An inverse relationship between extraction yields and antioxidant capacity of red seaweed was observed, and the authors suggested that the antioxidant capacity of seaweed is based on the combined effects of the extracted phenolic substances rather than the extraction yields [64]. Other constituents such as chlorophyll, flavonoid, and carotenoid may also influence the antioxidant activity of extracts from seaweed [60].

Sargassum polysaccharides also possess strong antioxidant capacity by enhancing the activities of superoxide dismutase, reducing glutathione, and glutathione peroxidase, thereby inhibiting oxidative stress in broiler chickens [66]. Sargassum can be found in Southern China, and its beneficial effects in traditional Chinese medicine have been established over the years [67]. Aside from antioxidant activities, Sargassum polysaccharides have shown immunomodulatory roles and the ability to combat deadly diseases in humans [67]. Fucoxanthin, a major carotenoid found in brown algae derived from Laminaria japonica seaweed, had a significant impact on chickens’ antioxidant capacity, evidenced by increased catalase, superoxide dismutase activities, and glutathione levels, and reduced malondialdehyde levels in the tissues; however, its effect on growth performance was insignificant [68]. A previous study investigated the relationship between the carotenoid, phenolic acid, and the antioxidant ability of fucoxanthin-producing algae and confirmed that the antioxidant ability is associated with carotenoid and phenolic acid [69]. In addition, the antioxidant mode of action of red seaweed has been previously studied. An in vitro study on Mastocarpus stellatus revealed that the antioxidant capacity of carrageenans, sulfated galactans, is related to the sulfate content [70]. Meanwhile, the molecular weight was reduced after polysaccharide extraction with acid and alkali [70]. This implies that the mode of extraction can influence the effects of seaweed on the antioxidant status of animals. Another study explored the nutritional and antioxidant components of three red seaweed species (Chondrus crispus, Mastocarpus stellatus, and Gigartina pistillata) and found that the three species had similar nutritional composition values [71]. Meanwhile, the inorganic contents were significantly different. On the antioxidant capacity, Chondrus crispus had the most excellent thiobarbituric acid reactive substances activity, followed by Mastocarpus stellatus and Gigartina pistillata. However, similar results were recorded in the case of the oxidative hemolysis inhibition assay [71]. Despite red seaweed bioactivities, the antioxidant effects in poultry birds are underexplored. The above studies demonstrated that the antioxidant ability varies in potency and is specific to each species of seaweed. Details on the antioxidant effects of seaweed are summarized in Table 2.

Type of seaweed	Scientific name	Dosage investigated	Effects	Dosage with optimum performance	Type of birds	Sample	Source of seaweed	Reference
Brown seaweed (meal)	Ascophyllum nodosum	2%	Did not influence antioxidant enzymes	none	Broiler chickens	Plasma and serum	Canada	[72]
Brown seaweed (extract)	Ascophyllum nodosum	1 ml/L, 2 ml/L in drinking water,	Did not influence antioxidant enzymes	none	Broiler chickens	Plasma and serum	Canada	[72]
ADP extracted from green seaweed	Enteromorpha prolifera	1000 mg/kg	Improved T-AOC, GS, reduced MDA in HS birds	1000 mg/kg	Indigenous broilers	Duodenum	China	[73]
Polysaccharide extracts from green seaweed	Enteromorpha prolifera	1000, 2500, 4000, 5500, and 7000 mg ADP/kg	Increased serum duodenum, jejunum, and ileum CAT, liver T-SOD, and decreased MDA	1000–7000 mg/kg	Broiler chickens	Serum, liver, small intestine	China	[57]
Polysaccharide extracts from green seaweed	Enteromorpha prolifera	1000, 2500, and 5000 mg/kg	Improved serum SOD jejunum SOD, liver CAT, reduce serum, jejunum, liver MDA	1000–5000 mg/kg	Laying hens	Serum, liver, jejunum	China	[74]
Extracts (dried alkaline and aqueous) from red seaweed	Kappaphycus alvarezii	0.5, 1.5, or 5.0 g kg⁻¹ diet	No effects on antioxidant enzymes	None	Broiler chickens	Serum	Bali, Indonesia	[75]
Ulvan is extracted from green seaweed	Ulva spp.	0, 0.05, 0.1, 0.5, 0.8, 1 (%)	Decreased MDA at 68 weeks	0.8%, 1%	Laying hens	Serum	China	[76]
Red seaweed	Kappaphycus alvarezii	1.25%, 1.5%, 1.75%	Reduced TBARS	1.75%	Laying hens	Egg yolk	India	[77]
Green and brown seaweeds	Ulva Fasciata and Sargassum Cinereum	1.5%, 3% BS 1.5%, 3% GS	Increased antioxidant enzymes	1.5%, 3% BS, GS	Quails		Egypt	[78]
Sargassum (brown seaweed) polysaccharides extract	Sargassum	25–800 μg/ml	Increased SOD, GPX, reduced ROS	800 μg/ml	Chicken	Blood	China	[66]
Fucoxanthin extract	Laminaria japonica	100 mg/kg 200 mg/kg	Increased CAT, SOD, GSH, reduced MDA	100 mg/kg 200 mg/kg	Broiler chickens	Bursa	ThinOgen™ (USA)	[68]
Fucoxanthin extract from brown seaweed	Cystoseira barbata	0.01%, 0.02%, 0.04%	Inhibited lipid oxidation	0.02 and 0.04%	Turkey	Liver, breast, and drumstick tissue	Tunisia	[79]
Polymannuronate from brown algae	Laminaria hyperborean, Macrocystis pyrifera, Lessonia nigrescens, and Ascophyllum nodosum	1, 2, 3, or 4 g/kg	No effects on the antioxidant status	None	Broiler chickens	Meat sausage	China	[80]
Brown seaweed powder	Sargassum siliquastrum	1%, 2%	High TAC, SOD, GPx, GR. Reduced TBARS	1%, 2%	Quails	Blood	Egypt	[81]

Table 2.

Antioxidant effects of different species of seaweed in poultry.

Abbreviations: T-AOC (Total antioxidant capacity), GS (Glutathione reductase), MDA (malondialdehyde), CAT (catalase), SOD (Superoxide dismutase), TBARS (Thiobarbituric acid reactive substances), GPX (Glutathione peroxidase), ROS (reactive oxygen species), HS (heat stress), ADP (Algae-derived polysaccharides).

3.2 Seaweed growth-promoting effects on poultry

The quality of feed is an integral factor to consider in ensuring poultry’s optimum performance [82]. Seaweed is known for its growth-stimulating effects [83], but its effects on growth performance have been inconsistent based on the literature.

Dietary supplementation of Ulva spp. increased feed intake and overall body weight gain of indigenous hens; still, the feed conversion efficiency and nutrient digestibility were unaffected [84]. Another study [85] showed that dietary supplementation with the combination of Ulva lactuca (3%) and Azolla (5%) improved body weight gain, shank length, and feed efficiency compared to birds fed with Ulva lactuca alone. In contrast, 1% and 3% Ulva lactuca did not affect feed intake, body weight gain, feed conversion ratio, and nutrient retention, but 3% Ulva lactuca improved the dressing percentage and breast muscle yield of broiler chickens compared to the control [33]. The improvement in the dressing percentage was associated with Ulva’s higher crude protein and amino acid (methionine). The nutritional evaluation of Ulva lactuca revealed 55.0% higher crude protein, 82% higher crude fiber, and 44% lower ME than the corn. Though the treatments did not affect growth performance, the authors further reported numeric improvement in body weight gain for birds fed with 3% Ulva lactuca compared to 1% Ulva lactuca [33]. A previous study revealed that supplementing 3.5% Ulva spp. meal had no adverse effect on visceral organ size, carcass characteristics, meat quality, and stability of indigenous hens. This indicates that green seaweeds cannot delay oxidation reactions in poultry meat [86]. More studies utilized the Ulva spp. in chicken feed than other types of seaweed, probably because of its high protein content. Ulva contains insoluble and soluble dietary fiber and is richer in proteins than other types of green seaweed. This indicates that Ulva can also serve as an alternative source of proteins for animal feeding [29]. Algae-derived polysaccharides from Enteromorpha improved the average daily gain and feed conversion ratio during days 1–21 and increased the final body weight compared to the control in broiler chickens [57].

Regarding brown seaweed effects, Mhlongo and Mnisi [87] found that the dietary addition of Ecklonia maxima meal up to 80 g/kg did not affect nutrient digestibility, growth performance parameters, and meat quality of local cockerels, but it improved the feed intake. Meanwhile, combining a type of seaweed with an enzyme (1.0% Laminaria japonica and 1% transglutaminase) positively affected the meat quality characteristics by improving the textural and sensory properties of the semi-dried chicken sausages [88]. Moreover, dietary supplementation of laminarin or laminarin/fucoidan extract from a brown seaweed (Laminaria digitata) improved feed intake and the growth rate of chickens in the post-hatch period [89]. Laminaria digitata is an abundant seaweed, rich in essential amino acids, carbohydrates, vitamins, and minerals [90]. Akinyemi and Adewole found that dietary supplementation of 2% brown seaweed meal (Ascophyllum nodosum) improved broilers’ growth performance parameters (average feed intake, body weight gain, and water intake), irrespective of the exposed heat stress challenge [72]. Another author observed that the dietary supplementation of phlorotannin extract from brown seaweed (Ascophyllum nodosum) had no negative effects on commercial broiler feed intake, growth, and mortality [45]. In addition, the final average body weight of birds fed with 15% Laminaria digitata (brown seaweed) and 15% Laminaria digitata + 0.01% recombinant CAZyme was 185 g lower than the control birds. The feed conversion ratio of birds that received the 15% Laminaria digitata was poorer than those fed a control diet, which implies that a high dose of brown seaweed can compromise a bird’s growth performance [90].

Dietary supplementation of red seaweed (1% Sarcodiotheca gaudichaudii and 1% Chondrus crispus) increased egg yolk weight and egg weight, respectively. Meanwhile, there was no significant effect on the growth performance parameters, feed intake and body weight, and egg production of laying hens [91]. Another study showed no significant differences in body weight on d 1, d 21, and d 32, but there was an improvement in feed intake and overall performance when broilers were fed with 0.3 and 0.4% Chondrus crispus at 22–32 days old. 0.3% Chondrus crispus also improved breast and carcass yield but decreased the abdominal fat of broilers [92]. Broilers’ feed intake was improved with the dietary addition of red seaweed from d 14 to 28. Overall, it improved the feed conversion ratio, while the body weight gain tended to increase in the seaweed-supplemented groups from d 14 to 28 and d 28 to 42 [93]. Another study also observed an increase in body weight gain in broiler chickens fed with Kappaphycus alvarezii [94]. Birds fed with an aqueous extract of red seaweed had 7% higher body weight than those fed with the dried alkaline extract. The aqueous extract of red seaweed had a higher concentration of total phenolic contents, phycobilins, scavenging activity, and trace materials compared to the dried alkaline extract [75]. This implies that the growth-promoting effects of seaweed are also influenced by the form of seaweed extract supplemented in the poultry diet. Mandal et al. [77] found improvement in laying hens’ production performance, shell thickness, and some internal egg qualities in response to Kappaphycus alvarezii powder (red seaweed) supplementation. However, egg production decreased as the inclusion levels of seaweed increased from 1.25 to 1.75%. The decreased performance observed in response to the higher inclusion of red seaweed is similar to the findings in chickens and fish. For instance, Al-Asgah et al. [95] observed a decreased feed intake and poor feed utilization among chickens fed with 20 and 30% of red seaweed (Gracilaria arcuata), while optimum performance was seen among the groups fed with 10%. Three percent Eucheuma denticulatum, a type of red seaweed, significantly improved juvenile fish’s growth rate and feed efficiency [96]. The authors observed negative effects on fish growth performance when fed with higher doses [95, 96]. This indicates that a high inclusion level of seaweed could harm animals. The growth-promoting effects of seaweed are associated with the presence of its polysaccharides, which may reduce its utilization at higher dosage levels [84]. Table 3 summarizes the effects of seaweed on the growth performance of poultry birds.

Type of seaweed	Scientific name	Dosage investigated	Effects	Best dosage with optimum performance	Type of birds	Source of seaweed	Reference
Red seaweed meal	Palmaria palmata	0.05, 0.1, 0.15, 0.20%	Linearly improved FI (d14–28), FCR (d28–42)	0.15%, 0.20%	Broilers	North Atlantic	[93]
Red seaweed powder	Chondrus crispus	0.3, 0.4%	Improved FI (d22–32), (d1–32).	0.3%, 0.4%	Broilers	Granma Province, Cuba	[92]
Red seaweed powder	Kappaphycus alvarezii	1.25, 1.5, 1.75%	Improved egg production	1.25%	Laying hens	India	[77]
Green seaweed meal	Ulva spp.	2, 2.5, 3, 3.5%	Improved ABWG Wk 5 and 13	2.5%	Indigenous hen	Cape Province, South Africa	[84]
Green seaweed meal	Ulva lactuca	1, 3%	Treatments did not affect BWG, FI, and FCR	None	Broilers	Egypt	[33]
ADP is extracted from green seaweed	Enteromorpha	1000, 2500, 4000, 5500, 7000 (mg/kg)	Improved average daily gain, FCR (D1–21), Body weight (D1–35)	1000 mg/kg	Broilers	China	[57]
Green seaweed pretreated with viscoenzyme	Ulva spp.	0, 0.2, 0.5, 0.75, and 1.2%	Treatment did not affect growth performance	None	Broilers	South Africa	[97]
Green seaweed	Ulva spp.	0, 20, 25, 30, and 35 g/kg	No effect on overall feed intake, growth performance, and carcass and meat quality traits. Decreased FCR	None	Broilers	South Africa	[83]
red seaweed and brown seaweed	Chondrus crispus (CC, Ascophyllum nodosum (AN)	0%, 3% CC, 0.5% AN	Seaweed decreased FI, BWG	None	Laying hens	Canada	[98]
Brown seaweed	Ascophyllum nodosum	1 and 2% seaweed	Improved BWG, FCR	2%	Turkey	Seaplant, Canada	[99]
Brown seaweed	Ascophyllum nodosum	0 ml, 1 ml/L of water	Improved BWG and FCR	1 ml/L	Broiler chickens	Not clearly stated	[100]
Brown seaweed	Not stated	0.5, 2, 3.5, and 5%	Increased BW, BWG, and performance index.	3.5%	Broiler chickens	Not clearly stated	[101]
Brown seaweed	Ascophyllum nodosum	1, 2 ml/L (extract), 2% seaweed meal	Improved growth performance parameters	2% seaweed meal	Broiler chickens	Canada	[72]
Brown seaweed	Ascophyllum nodosum	5, 10, 20 (g/kg)	No dietary treatment effects	None	Broiler chickens	Greece	[102]
Brown seaweed	Sargassum siliquastrum	0, 1, 2 (%)	Better FCR, lowered mortality	1%, 2% (FCR), 2% reduced mortality	Quails	Egypt	[81]
Brown seaweed	Saccharina latissima	0.6% algal meal 0.08% algal extract	Higher BW on days 3, 7, and 37 post-hatch	0.08% algal extract	Broiler chickens		[103]

Table 3.

Growth-promoting effects of different species of seaweeds.

Abbreviations: FI, feed intake; FCR, feed conversion ratio; ABWG, Average body weight gain; BW, body weight; BWG, body weight gain; ADP, Algae-derived polysaccharides; d, day; Wk, week.

3.3 Functional roles of seaweed on poultry immune health

Seaweeds have positively enhanced the immune function and intestinal health of poultry [81, 90]. Specifically, on brown seaweed, dietary supplementation of 15% Laminaria digitata increased jejunum, ileum, and cecum lengths, which shows brown algae’s potential for increasing nutrient absorption and modifying intestinal morphology, despite the growth impairment caused by its inclusion in the diet [90]. In contrast, laminarin extract from Laminaria digitata supplemented at 0.057 and 0.114% in broiler chickens did not influence vaccine-induced antibody responses nor intestinal development [104]. The supplementation of brown seaweed, Sargassum siliquastrum, in quails’ diet enhanced the duodenal villus:crypt ratio, villus height and width, and IgA, IgG, and IgM concentrations compared to the control diet. Further results revealed that 1 and 2% Sargassum siliquastrum increased cecum length by 8.13% and 7.70% and weight of intestine by 9.07 and 9.45%, respectively, compared to the control diet [81]. Sargassum siliquastrum improved the growth performance and nutrient digestibility of quails by strengthening their intestinal integrity and immune system [81]. Similarly, Sargassum spp. at 1 and 2% significantly increased IgA antibody titer in broiler chickens compared to other dietary groups (5%, 7.5% Spirulina, 0.5%, 1% Gracilaria spp.) [105]. Chavan et al. [106] found that Sargassum wigette supplemented at 0.13% significantly improved the cell-mediated immunity and reduced pathogenic bacteria in broiler chickens. Kereh et al. [107] showed that the uronic acid extracted from Sargassum crassifolium (brown seaweed) increased the immunity of Lohman chicken eggs and could further inhibit viral replication by forming antibodies. Choi et al. [108] compared different forms of seaweed (brown seaweed byproduct, fermented brown seaweed byproduct, seaweed fusiforme byproduct, fermented seaweed fusiforme byproduct) and found that the dietary treatments improved the concentration of IgA in chickens except for the fermented brown seaweed byproduct. Meanwhile, IgM concentrations were higher in the fermentation groups compared to the non-fermented ones. Moreover, 0.2% sodium alginate extracted from brown seaweed induced interferon-γ, IL-10, and IL-1β in the cecal tonsils of unchallenged birds, which indicates the immunological roles of seaweed in the maturation of the humoral immune system [109].

On green seaweed, laying hens fed with Enteromorpha prolifera-supplemented diets had higher serum antibody titers of Newcastle disease and lymphocyte transformation rate of blood, reduced number of Escherichia coli and increased Lactobacillus population compared with the control group [110]. Dietary 2500 mg/kg polysaccharides from Enteromorpha improved the jejunum and ileum villus height of broiler chickens on d 21, and dietary 4000 mg/kg algae-derived polysaccharide (ADP) increased the villus height in the duodenum and ileum on d 35. Results on intestinal permeability revealed that 1000–7000 mg/kg of the polysaccharides decreased diamine oxidase activity and D-lactic acid on d 21 and 35 [57]. Further results showed that 1000 mg/kg ADP up-regulated the mRNA expression of IκBα and down-regulated the mRNA expression of NF-κB p65, TNF-α, and IL-6 in the bursa of Fabricius of heat-stressed chickens. 1000 mg/kg ADP restored infiltrated inflammatory cells, cell structure, necrosis, and ameliorated histological damage among heat-stress birds [73]. The addition of Ulva rigida (green algae) improved the intestinal health of broilers, evidenced by an increase in villus height and width, but had no effect on the body weight gain and carcass percentage [111]. One percent ulvan supplementation showed a positive effect on interleukin-6 and 0.8% of ulvan on interferon-γ at 68 weeks in laying hens [76]. The immunomodulatory activity of Ulva spp. is closely related to their low molecular weight and sulfate content. Ulvans act as immunodulatory agents through various mechanisms, including suppression of proinflammatory cytokines, enhancement of anti-inflammatory cytokines, and restoration of gut microbiota balance [112].

Dietary supplementation of red seaweed (Palmaria palmata) also improved the intestinal mucosa functionality of broilers, evidenced by jejunal villus height and width compared to the control. The weight of the bursa of Fabricius increased linearly with increasing inclusion levels (0.05, 0.1, 0.15, and 0.2%) [93]. Mandal et al. [77] showed that increased levels of red seaweed, Kappaphycus alvarezii, from 1.25 to 1.75% improved the cell-mediated and humoral immunity in laying hens. Likewise, the humoral immunity was improved among birds treated with 1.0 g/kg aqueous extract of Kappaphycus alvarezii, coupled with higher expression of intestinal claudin 2, TLR2A, NOD1, avian beta-defensin 4, interleukin 2 and 6 genes and 1.5 g/kg improved villus width and crypt depth compared to the control [75]. Generally, the above seaweed immunomodulatory activity ascertained the presence of active compounds that can promote resistance to diseases. An important mechanism of action is that seaweed polysaccharides can stimulate intestinal epithelial cells to produce cytokines that initiate and enhance protective immune responses of the animals against pathogens [113].

3.4 Antimicrobial mode of action of seaweed in poultry

Seaweeds are considered a potential prebiotic, which can enhance nutrient absorption, improve gastrointestinal health, and potentially replace antibiotic use in poultry production [16]. Seaweed polysaccharides, such as carrageenans (red seaweed), laminarin and fucoidan (brown), and ulvans and mannans (green), are resilient to digestion in the upper gastrointestinal tract but serve as a substrate for bacterial fermentation in the colon, stimulating immune-modulatory effects in animals [31]. Studies have examined the antimicrobial effects of various seaweed polysaccharides in poultry birds. For example, laminarin extract from Laminaria hyperborea was tested against four bacteria pathogens, including Staphylcoccus aureus, Listeria monocytogenes, Escherichia coli, and Salmonella typhimurium. The authors established that the acid extracts had better inhibition capacity against bacterial growth compared to water extracts. Ascophyllum nodosum extracts completely inhibited Salmonella typhimurium’s growth, while the acid extract of Ascophyllum nodosum effectively inhibited the bacterial growth of all species [114]. Considering the different types of seaweed observed in this study [114], Laminaria hyperborean was found to have higher laminarin and phenolic contents than Ascophyllum nodosum. The highest content of phenolics in Laminaria hyperborea was 0.365 mg PGE/gdb, while that of Ascophyllum nodosum was 0.166 mg PGE/gdb. This justified why Laminaria hyperborean exhibited higher antimicrobial activity than the other species. This result suggested that laminarin from brown seaweed, extracted using acidic solvents, can function effectively as an antimicrobial constituent in poultry nutrition. A researcher previously found that laminarin or laminarin/fucoidan extract from brown seaweed (Laminaria digitata) did not affect the colonization of the bacteria pathogen, Campylobacter jejuni, though it promoted the expression of key genes involved in immune response and improved growth performance of chicks [89]. The method of extraction was not clearly stated. Nofal et al. [115] found that methanol extract of Sargassum muticum significantly inhibited the growth of Salmonella typhimurium, Escherichia coli, Bacilli, and Staphylococcus aureus compared to the control. The antimicrobial function of the methanol extract was found to be more effective than that of the aqueous extract. Further phytochemical analysis revealed the presence of secondary metabolites such as flavonoids and phenolic compounds in Sargassum muticum, which is responsible for the antibacterial activity [115]. Bonifait et al. [45] revealed that the dietary supplementation of phlorotannin extract from brown seaweed (Ascophyllum nodosum) did not reduce Campylobacter colonization in broilers. Yan et al. [109] found that the inclusion of sodium alginate oligosaccharide extracted from brown seaweed at 0.2% effectively inhibited the colonization of Salmonella in the chicken ceca by enhancing the growth of lactic acid bacteria. In Japanese quails, dietary supplementation of 1 and 2% Sargassum siliquastrum increased the abundance of Lactobacillus in the cecum but decreased that of pathogenic bacteria: E. coli and C. perfringens [81]. All the above studies affirmed that brown seaweed polysaccharides could regulate the gut microbiota. The short-chain fatty acids, which are vital metabolites of brown seaweed polysaccharides, can enrich the gut microbiome by enhancing the growth of beneficial bacteria and preventing that of harmful ones [116]. The antimicrobial ability of different polysaccharides from the same species of seaweed seems to differ.

On red seaweed effects, Kulshreshtha et al. [117] tested six species (Chondrus crispus, Gymnogongrus devoniensis, Palmaria palmata, Sarcodiotheca gaudichaudii, Solieria chordalis, and Sarcodiotheca spp.) for antimicrobial activity against Salmonella Enteritidis. The extracts from Sarcodiotheca gaudichaudii and Chondrus crispus significantly reduced the growth of Salmonella Enteritidis, exhibiting excellent antimicrobial properties. Two percent supplementation of Sarcodiotheca gaudichaudii and Chondrus crispus improved the ileal villus height and surface area of laying hens compared with the control diet [91]. The addition of red seaweed also enhanced the growth of beneficial bacteria such as Bifidobacterium longum, Streptococcus salivarius, increased the concentrations of short-chain fatty acids, and reduced the dominance of harmful bacteria (Clostridium perfringens) in the chicken gut community [91]. Kulshreshtha et al. [118] affirmed that dietary inclusion of Chondrus crispus prevented the colonization of Salmonella in the excreta and ceca, possibly by promoting the growth of Lactobacillus and increasing the concentration of short-chain fatty acids such as butyrate. More analysis showed a linear increase in Lactobacillus sp. counts and a decrease in E. coli counts on day 42 among chickens fed with red seaweed (Palmaria palmata) [93]. This review showed that seaweed promoted the activity of beneficial bacteria while reducing that of pathogenic ones, which supported previous assertions that seaweed is an excellent prebiotic for poultry health.

4. Risks and toxicity considerations in seaweed-based poultry feed

One of the major safety concerns regarding the use of seaweed in animal feed is the bioaccumulation of heavy metals such as arsenic (As), cadmium (Cd), and lead (Pb) [119]. Seaweeds, especially those growing in coastal and estuarine environments, easily absorb metals from the surrounding water and sediments. Chen et al. [120] examined the concentrations of heavy metals in Porphyra (a red seaweed) and Laminaria (a brown seaweed) cultivated in a coastal city in China. Their analysis revealed that Pb levels in all samples were below the legal limit established in France, while Cd and Hg concentrations in Laminaria were within the safety thresholds set by the European Union. Overall, Porphyra samples tended to exhibit higher concentrations of Pb and Cd compared to Laminaria. Anbazhagan et al. [121] found that the metal concentrations for red and brown seaweeds from the Tuticorin coast of the Gulf of Mannar, India, were majorly Pb, Zn, Cu, Cd, of which Cd and Pb levels were found to be elevated in both the red and brown seaweeds. Another study observed that seaweed heavy metal contents varied between species and collection sites with minimal seasonal variations [23]. Total As was higher in kelp than in the Palmaria (Saccharina > Alaria > Palmaria). Both the Cd and Pb concentrations were highest for Alaria, and similarly low for Saccharina and Palmaria [23]. Regarding the collection site, seaweeds from France had the highest As, Hg, and Pb, but the lowest Cd, while Norway samples contained the highest Cd, but the lowest As and Pb [23]. A similar report showed the highest levels of cobalt, chromium, iron, manganese, nickel, and selenium in Swedish sugar kelp, while sodium and zinc were highest in Norwegian samples [122]. On safety concerns, Roleda et al. [23] found that the heavy metal (As, Cd, Hg, Pb) concentrations in two brown seaweeds (Saccharina latissima and Alaria esculenta), and the red seaweed, Palmaria palmata, were below the upper limits set by the French recommendation and the EU Commission Regulation on contaminants. Although certain seaweed species contain high metal concentrations, health risk assessments have consistently shown that their consumption poses a low risk to human and animal health. Roleda et al. [23] reported a low health risk associated with heavy metals in edible seaweeds, while a similar assessment by Anbazhagan et al. [121] confirmed that, despite elevated levels of Cd and Pb, the calculated hazard index remained below critical thresholds.

In addition, high levels of iodine found in some brown seaweeds (ranging from 1500 to 8000 ppm) may be another potential hazard that limits seaweed consumption [21]. Brown seaweed, especially Laminaria, can accumulate iodine over 30,000 times higher than that found in seawater [31]. Brown algae may cause iodine toxicity when fed during prolonged periods. Unlike brown algae, red seaweed contains small amounts of iodine (0.03–0.04%) [31, 123]. The maximum iodine concentration proposed in complete feeds for laying hens is 3 mg/kg [124]. According to NRC (1994), iodine dietary requirements were established to be 0.35 mg/kg for broilers, 0.5 mg/kg for layers, and 0.4–0.5 mg/kg for Turkeys. Although some seaweed contains high concentrations of iodine, its inclusion in animal feed does not necessarily pose a risk of excessive iodine intake when used within recommended regulatory limits. Iodine is an essential nutritional element required in very minute amounts by animals and plays a major role in cell differentiation, growth, and development, and the regulation of metabolic rates in animals [125]. Careful harvesting and post-harvest handling, and drying could help with consistent delivery of a uniform quantity of iodine. To ensure poultry health, it is essential to routinely screen seaweed sources for heavy metals and ensure they comply with established safety standards, as exposure to these contaminants can adversely affect growth, immunity, and overall performance.

Post-harvest processing is one of the strategies for reducing undesirable compounds in seaweed intended for animal or human consumption. For example, studies on Saccharina latissima (a brown seaweed farmed and processed in Norway) have shown that blanching is effective in significantly reducing iodine concentrations. Further fermentation of blanched seaweed further decreased iodine content, inorganic As, Zn, and Cd, thereby enhancing the safety of the seaweed [126]. Jönsson et al. [122] observed that different processing methods, including ultrasound, heat-assisted extraction, blanching, soaking seaweed in water and acid, and high pressure, reduced some toxic elements in Saccharina latissimi, with up to 92.4% inorganic As, 72.8% iodine, and 49.4% Pb removed. Heat-assisted extraction was the most effective, reducing all contaminants to the greatest extent. Noriega-Fernández et al. [127] found that the combination of ultrasound and EDTA at 50°C for 5 min significantly reduced As (32%), Cd (52%), and iodine (31%) content in Laminaria hyperborea, thus improving the safety of seaweed for consumption. A different study reported that soaking treatments in warm fresh water (32°C) reduced the iodine in Saccharina latissima, and treatment of Alaria esculenta in hypersaline solution (2.0 M NaCl) reduced the relative Ca content. However, both treatments affected the nutrient content of seaweed [128]. In addition to nutrient loss, improper processing of seaweed can pose microbial risks. Banach et al. [126] reported the detection of Bacillus cereus in both blanched and fermented seaweed samples and the introduction of Vibrio alginolyticus during the blanching process itself, indicating that contamination can occur not only during post-harvest but also at the early stages of processing, particularly if blanching water or surfaces are not properly sanitized. In general, processing methods must be carefully optimized to balance safety and nutritional value for feed applications.

5. Challenges to the effectiveness of seaweed on poultry health

Undoubtedly, the bioactivity of seaweed suggests that a seaweed-supplemented diet could improve the antioxidant capacity, immune system, and overall growth performance in poultry birds. Considering the literature reports on seaweed performance, the biological activities are not directly proportional to the effectiveness that has been recorded. This section focuses on some drawbacks to seaweed usage.

Utilization challenges due to the presence of anti-nutritional factors, such as non-starch polysaccharides, tannins, and phytates, can reduce nutrient absorption, hence affecting growth performance. High inclusion of cellulose and hemicellulose can negatively affect digestibility [97]. Past studies have reported a decrease in birds’ performance with increasing inclusion levels of seaweed [77, 83, 129]. Optimum inclusion levels of different types of seaweed should be established to maximize their effects on poultry health and performance. Table 4 lists optimal dosage ranges of seaweeds in poultry diets based on previous studies.

Seaweed species	Optimal inclusion rate (% of diet)	Biological activity	Poultry type	References
Enteromorpha prolifera (Green)	0.1%	Improved antioxidant ability. Inhibited lipid oxidation	Indigenous broilers	[73]
Enteromorpha prolifera (Green)	0.1–0.7%	Improved antioxidant ability. Inhibited lipid oxidation	Broiler chickens	[57]
Kappaphycus alvarezii (Red)	1.75%	Reduced TBARS	Laying hens	[77]
Cystoseira barbata (Brown)	0.02 and 0.04%	Inhibited lipid oxidation	Turkey	[79]
Sargassum siliquastrum (Brown)	1, 2%	Improved antioxidant ability. Reduced TBARS	Quail	[81]
Ascophyllum nodosum (Brown)	2%	Improved growth performance	Turkey	[99]
Ascophyllum nodosum (Brown)	2% seaweed meal	Improved growth performance parameters	Broiler chickens	[72]
Ulva spp. (Green)	2.5%	Improved growth performance parameters	Indigenous hen	[84]
Kappaphycus alvarezii (Red)	1.25%	Improved egg production	Laying hens	[77]
Sargassum spp. (Brown)	1, 2%	increased IgA antibody titer	Broiler chickens	[105]
Sargassum siliquastrum (Brown)	1, 2%	Increased the abundance of Lactobacillus. Decreased pathogenic bacteria	Quails	[81]
Green seaweed	0.75, 1.00, and 1.25%	enhances immune response by increasing IgA and IgG levels	Broiler chickens	[130]
Ascophyllum nodosum (Brown)	2% seaweed meal	Improved beneficial microbes	Broiler chickens	[131]
Ascophyllum nodosum (Brown)	0.125, 0.25%	Improved growth performance	Broiler chickens	[132]
Palmaria palmata (Red)	0.15, 0.20%	Improved growth performance	Broilers	[93]

Table 4.

Optimal dosage ranges of seaweeds in poultry diets.

Abbreviations: TBARS (Thiobarbituric acid reactive substances), IgA (Immunoglobulin A), IgG (Immunoglobulin G).

Seaweed chemical composition varies greatly and could be influenced by seasonal changes and geographical location, which might affect the effectiveness of seaweeds. For instance, carbohydrate and protein concentrations of Sargassum wightii were highest in March, and minimal values were recorded from July through September. Maximum ash contents (22.3 ± 0.12%) were recorded in July, and minimum (16.2 ± 0.08%) in November [133]. Ascophyllum nodosum collected in October showed low polyphenols and ash contents, while the highest polyphenol content was recorded in the summer months [134]. Another study on Irish seaweed species (Fucus serratus, Ascophyllum nodosum, Himanthalia elongata, Laminaria digitata, and Palmaria palmata) showed that pigment levels and polyunsaturated fatty acids (PUFA) generally decreased in summer and were associated with a higher ratio of xanthophylls to chlorophylls [135]. Seasons also influenced the antiproliferative activity of Sargassum oligocystum. The highest antiproliferative activity of Sargassum oligocystum was found in samples collected during the monsoon season (August), compared to February (the hot/dry season), May (the early monsoon season), and December (the cool/dry season) [136]. Seasonal differences should be considered while harvesting seaweed to obtain a specific composition [137] and maximize the effectiveness of seaweed for specific applications in the feed industry.

On geographical location, Rødde et al. [138] showed clear geographic and seasonal differences in the composition of seaweed samples collected from Portaferry (Northern Ireland), Galway (Ireland), Oviedo (Spain), and Trondheim (Norway). Protein content reached up to 30% of dry weight, with region-specific seasonal peaks (spring in Portaferry and winter in the other sites). Floridoside accumulation was also site-dependent, peaking in summer in Trondheim and Oviedo, in autumn in Galway, and showing no distinct peak in Portaferry, likely due to elevated nitrogen availability in the water. Another study observed spatial and seasonal differences in the nutritional composition of six dominant seaweed species. Fiber content ranged from 26.5 to 53.5% of dry weight (dw) and varied significantly with site and season. Carbohydrates (8.4–25.3% dw) were positively correlated with seawater temperature, salinity, and pH. Lipid content was lowest in spring (0.6% dw) and highest in winter (1.1% dw), with variations influenced by nitrite and pH levels [139]. All these factors affect the nutritional and biological function of seaweeds, which is critical for their utilization in animal feed applications.

The extraction approach also influenced the antiproliferative activity of Sargassum oligocystum, with the lipophilic extract showing greater efficacy compared to ethanolic, acidic, and alkali extracts in this season [136]. It was reported that ultrasound produced higher laminarin content from brown seaweed compared to the conventional solid-liquid extraction [114]. Further analysis showed that laminarin extracted from Laminaria hyperborea using ultrasound had a higher molecular weight (3242–5052 Da) compared to that extracted by other methods. This implies that the ultrasound method is more effective than the solid-liquid approach for extracting higher molecular weight laminarins. The extracts obtained with acid had higher antioxidant capacity compared to extracts from the water solvent method, while the liquid method was better in the extraction of phenolics [114]. Two extraction methods were previously used to maximize the yield and concentration of different species of red seaweeds; conventional heat-assisted extraction was more efficient than high-pressure-assisted extraction [71]. An in vitro and in vivo study found that the ensiling, washing, and extraction processes also reduced the nutritional value of seaweed, organic matter, and nitrogen digestibility, which makes it unsuitable for broilers’ diet [140]. Wang et al. [141] observed that the crude extract of Sargassum silliquosum had a higher antioxidant ability with an effective concentration (EC₅₀) of 0.34 mg/ml 2,2 diphenylpicrylhydrazyl (DPPH) compared to the purified fucoidan (EC₅₀ of 2.58 mg/ml DPPH) obtained from Sargassum silliquosum. Conversely, purified fucoidan showed higher anti-inflammatory ability compared to the crude extract [141]. Chan et al. [64] determined the effect of the activity of different solvent extracts (methanol, ethanol, water, acetone, ethyl acetate extract) on Gracilaria changii (red seaweed), the ethanol and methanol method had the highest extraction yield (13.06 ± 1.14%) followed by water (12.36 ± 0.76%) and ethyl acetate extract resulted in the lowest yield (3.15 ± 0.45%). Additional results showed that ethyl acetate extract showed the highest scavenging capacity with an EC₅₀ of 0.51 ± 0.09 mg/ml, with the highest total phenolic contents of 21.57 ± 2.58 mg/PGE compared to other extraction methods [64]. The yield and the nutritional value of extracted compounds are directly linked to the extraction procedures, which can alter the functional properties of seaweed. More studies should evaluate aqueous, ethanolic, and enzymatic extractions for yield, bioactivity, and safety. Enzymatic extraction often preserves sensitive compounds and improves digestibility, while ethanol may concentrate phenolics but is less sustainable for feed applications.

Another challenge to the effectiveness of seaweed on poultry health is the impact of drying on the nutritional and bioactive compounds of seaweeds. Uribe et al. [142] found that the drying process had a significant effect on the total phenolic and flavonoid contents of brown seaweeds. Convective drying samples had the highest vitamin contents and phytochemicals, while freeze-drying seaweed exhibited the best pigment retention compared to vacuum, infrared, and solar drying methods. Figure 3 summarizes the challenges to the effectiveness of seaweed and its impact on poultry health.

Figure 3.
Challenges to the effectiveness of seaweed and its impact on poultry health.

6. Potential solutions to challenges

Reported studies indicated that seaweeds have a plethora of benefits and contributions to poultry production. However, further development in the effectiveness of seaweeds continues to face several constraints and challenges. High dosage rates of green seaweed may negatively affect nutrient digestibility due to indigestible algae cell wall polysaccharides [143]. Pre-treatment with, or the addition of, enzymes could potentially degrade the cell wall, hence improving digestibility and absorption. Costa et al. [90] found that a Laminaria digitata diet supplemented with carbohydrate-active enzymes (CAZymes) reduced intestinal viscosity and negative effects on broilers’ growth performance caused by 15% macroalgae in feed and showed positive effects on meat quality parameters. The supplementation of Ulva lactuca with carbohydrases also reduced ileal viscosity, with potential beneficial effects on broiler digestibility [143]. Stokvis et al. [144] found that enzyme treatment did not affect nutrient digestibility but increased the ash content of chickens. Disruption methods like bead milling or high-pressure homogenization with enzymatic pre-treatment, using cellulases prior to algal compound extraction, may increase the yield and bioavailability of lipids, pigments, and minerals, and also enhance amino acid absorption [145]. The anti-nutritional factors and indigestible nutrients of seaweed can be mitigated by processing methods, including washing, powdering, fermentation, enzymatic treatment, and extraction of specific target compounds [146]. The combination of seaweed with other bioactive substances in poultry diets could also improve its efficacy. Three percent Laminaria japonica (brown seaweed) combined with 300 mg/kg cecropin (antibacterial peptides) distinctively improved the feed conversion ratio and immune function (lymphocyte ratio and blood Newcastle disease antibody titers) of broiler chickens. The co-supplementation of brown seaweed and cecropin further suppressed E. coli and increased Lactobacillus colonization in broiler chickens [147]. To achieve acceptable yields for extract, extraction and purification techniques that can improve the final product of seaweed should be adopted [148]. Table 5 summarizes specific and actionable guidelines for poultry farmers. There is a need for long-term studies assessing the cumulative effects of seaweed consumption on poultry health, organ integrity, immune function, and growth performance. These studies would help to determine safer inclusion levels and reveal any risks that may not be evident in a short-term feeding trial.

Category	Guidelines
Selection of seaweed	Consider factors such as nutrient composition, digestibility, etc. Brown: Laminaria, Ascophyllum: Rich in polysaccharides Red: More digestible Green: High in minerals
Sourcing of seaweed	Prefer cultivated over wild-harvested seaweed
Storage and handling	Prevent contamination during storage and handling.
Post-harvest handling	Maintenance of good hygiene to prevent cross-contamination
Collection of seaweed	Collect seaweed in August to yield maximum content [149]
Final products	Avoid unprocessed seaweed
Inclusion levels	Up to 5% of the total diet. Monitor the bird’s response to avoid any adverse effects.
Implementation	Start with small-scale trials before full integration
Regulatory compliance	Ensure compliance with limits for heavy metals and iodine. Follow EU, CFIA standards as applicable

Table 5.

Specific and actionable guidelines for poultry farmers.

7. Conclusion

This review has comprehensively examined the bioactive compounds of seaweeds, highlighting their biological roles and potential health benefits in animal health applications. Seaweed composition and its polyphenol content make it a strong antioxidant that can scavenge free radicals and combat oxidative stress. Our findings showed that the antioxidant ability of seaweed varies in potency and is species-dependent. The divergences observed in different studies on the seaweed effect could be attributed to the variability in the nutritional composition of various species of seaweeds. The brown seaweed species is the most widely studied, while the red seaweed species is underutilized in poultry feeding. Nonetheless, red algae supplementation outperformed brown and green algae in achieving optimum growth performance in chickens, especially at lower inclusion levels. This might be associated with the higher protein content in red algae. More studies should investigate the effects of the three types of seaweeds as a combined diet. The combination of seaweed with enzymes or other plant materials might effectively improve the growth performance of chickens. Poultry studies should explore specific bioactive substances in seaweed rather than whole seaweed. Factors such as seasonal variation, location, and extraction methods could impact seaweed’s nutritional value and ultimately affect its efficiency. Proper extraction methods should be adopted while extracting polysaccharides from seaweed to maintain their biological activities. Ultrasound-assisted extraction is more effective compared to the traditional extraction method. The quality and effectiveness of extracted compounds depend on the extraction methods. New approaches should be adopted to obtain bioactive substances with high-quality yields. Further studies should involve the use of new extraction methods such as ultrasound, enzymes, and microwave-assisted technology rather than conventional methods. Moreover, to maximize the antioxidant activity of seaweeds, the focus should be based on specific phenolic compounds rather than total phenolic compounds.

Conflict of interest

The authors declare no conflict of interest.

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