4.2.1. Pine Nut Syndrome
In 2001, Mostin first introduced the term ‘Pine Nut Syndrome’ (PNS) in the literature as a taste disturbance [13
]. Pine nut syndrome is also known as pine mouth syndrome (PMS) or pine nut mouth syndrome [17
]. Kwegyir-Afful et al. [47
] introduced the term ‘Pine Mouth Event’. Medically, it is known as dysgeusia, metallogeusia or cacogeusia [10
According to Hampton et al. [48
], the initial symptom is a persistent metallic or bitter taste starting within hours to the first two days after eating pine nuts and can last for up to 14 days. In exceptional cases, the metal or acid taste could last for a maximum of 42 days [48
]. These pine mouth events went unnoticed by the scientific community until cases reported by pine nut consumers rose dramatically between 2008 and 2012 [27
]. Consequently, several studies tried to investigate the taste disturbance due to ingestion of pine kernels.
Apart from health aspects, lipids in pine nuts are of special importance due to their use in identification of species causing the syndrome. Senter et al. [49
], in their gas-liquid chromatography-mass spectrometry experiment, suggested that phenolic acids in pine nuts (1.37 µg g−1
) are relatively higher than in almonds (1.08 µg g−1
), filberts (0.36 µg g−1
) and black walnuts (0.51 µg g−1
). Phenolic compounds might be the potential reason for taste disturbance as these possess an astringent quality [49
]. Weise [51
] stated that the pine mouth events can happen due to rancidity of lipids. Destaillats et al. [12
] negated association of PNS to the oxidative reactions [36
] of lipids identified in their gas liquid chromatography analyses. It was also shown by Destaillats et al. [12
] that the total composition of fatty acids in Chinese kernels (P. armandii
) did not differ markedly from the other pine species in their experiment. From these studies, Köbler et al. [50
] inferred that the fatty acid composition of pine nuts does not influence taste disturbance. Möller [24
] proposed that PNS may be due to an elevated level of bile juice, which is produced as a result of bioactive compounds in pine nuts. The effect might be compounded by enterohepatic recirculation, which dramatically extends the residence time of many chemicals or drugs in the digestive tract.
No toxin, fungus, pesticide component or heavy metal had been evaluated as a direct reason for generating PNS [36
]. To the best of our knowledge, none of the studies (Table 5
) provided a relevant single cause for PNS development, though reliable methods were used, such as gas liquid chromatography [12
], fatty acid analysis and DNA testing [37
], and/or nuclear magnetic resonance analysis [50
] to identify pine nut species from the reference samples. Even the most extensive study on PNS conducted in France by Flesch et al. [45
], proved unhelpful in this regard. Flesch et al. [45
] suggested that the bitterness might be caused by an unknown toxin. The toxin seemed to them to be heat resistant. PNS is more frequent in females than males. They also hypothesized that this taste disturbance might be due to a polymorphism in the genetic expression of taste functions.
In addition to PNS, Hampton et al. [48
] briefly introduced the term anaphylaxis. For further details regarding anaphylactic reactions, Cabanillas and Novak [26
] have reviewed the issue quite clearly.
Most of the research in forestry dealt with pine trees (e.g., mainly ecology, historical aspects, and tree health issues) rather than pine nuts. P. armandii Franch was often presented in the literature as the most notorious species connected to PNS. This species grows in and comes directly from China.
It is very important to understand the true value of forest products so that they are utilized sustainably and, if necessary, protected for harnessing future benefits. Most of the studies found during the course of the present review were associated to PNS. Fortunately, we found some literature related to the economic valuation of this nutritious product.
Masiero et al. [52
], grouped 21 countries of the Mediterranean region into four sub-regions. This arbitrary grouping was done to better estimate values for a selected set of products including wood and non-wood forest products. Secondary data sources such as national reports, the FAO forest resource assessment report published in 2010, and seven additional papers were used to derive pine nuts results [52
] (pp. 4–10). The pine nuts considered by Masiero et al. [52
] were limited to P. pinea
. The minimum and maximum economic values for the different product ranges of pine nuts were estimated. The two alternative scenarios were developed from the International Nut and Dried Fruit Council’s report (min scenario) and the Mutke et al. (max scenario) paper published in 2012. The values estimated were 83.8 M€ to 307.7 M€ for producing 5295 tons to 18,992 tons of pine nuts. According to Masiero et al. [52
], FAO Forest Resource Assessment (2010) indicated a market value of 48.7 M€ for the production of 16,545 tons of shelled pine nuts. Lebanon and Tunisia were regarded as important producers with respect to the minimum production scenario and Spain performed best when the maximum production scenario was applied.
Unfortunately, the Masiero et al. [52
] study does not provide a holistic picture of different pine nut species. This is due to its specific focus on Mediterranean pine nuts. However, limitations due to a lack of official statistics and informal market channels for pine nuts justify the study.
Another study by Mutke et al. [27
] also addressed and emphasized the importance of Mediterranean stone pines (P. pinea
). A forest owner can obtain higher profits from pine nuts than harvesting timber in the Mediterranean region. In contrast to timber harvesting, revenue can be collected annually by selling pine kernels without waiting for the long pine rotations. In semi-arid sandy and/or rocky Mediterranean areas, the mean annual production of cones ranges 100–1000 kg ha−1
which can potentially yield 4–40 kg shelled pine nuts. So, prices in the world market are high enough (50–60 € kg−1
) to return an average income of 200–2400 € ha−1
A number of challenges along the European nuts’ supply chain were of special interest in the paper by Mutke et al. [27
]. It was noted that legal and commercial differentiation of those available on the market was without clear declaration of origin and species but under the generic name ‘pine nuts’. For instance, in Germany P. koraiensis
(Chinese nut) and P. gerardiana
(Pakistani nut) were sold under the name Pinienkerne
(general name for pine nuts in the German language). Similar issues were raised by Ballin and Mikklesen [42
], who found P. armandii
packed together with many other pine nut species.
The Sandeman Seeds Company labelled the UK as originator of those packets. However, we know that P. armandii
nuts grow and come mainly from China. Mutke et al. [27
] attributed confusion in detecting geographical origin of pine nuts to the concept of economies of scale (efficiencies formed by volume) rather than economies of scope (efficiencies formed by variety). This is due to a number of reasons such as the small size of pine nuts, dependence on a single product and supply, and current commercial and market structure. In our opinion, these issues most probably just happened due to re-exporting and re-importing of pine kernels.
The advent of modern device technology (mobiles and computers), internet, social networks and online news articles debating PNS have started to negatively affect trade and market development of pine nuts [27
]. Although the international collection of food standards ‘Codex Alimentarius’ has categorized pine nuts in TN 0673 since 1993 [8
], a clear system is still lacking for classifying the most important commercial species of pine nuts.
In some parts of the world, pine trees are mainly intended to better meet local consumption [8
]. However, pine nuts might cause problems out of their native region. For instance, pine nuts imported in the US are the main cause of PNS establishment because of their mixed nature [39
]. This is because pine nuts are difficult to distinguish morphologically. P. gerardiana
is very similar to P. pinea
. Similarly, P. sibirica
resembles P. armandii
. Ultimately, re-exports among several countries mask the traceability of origin and quality of the product. This is especially true when foreign suppliers normally sort and grade (from company A to C instead of B) pine kernels based on the number of pine nuts per 100 g. Business as usual varies greatly based on seed sizes e.g., 650–750 nuts/100 g to 1500–1700 nuts/100 g [58
]. This is why when pine nuts are purchased from a local market, species and geographical origin information is seldom on the packets.
As mentioned earlier, the number of reported cases of PNS started to increase in 2009. We have identified the following reasons in both the scientific as well as grey literature that might be directly or indirectly responsible. Contributing factors may be a combination of the following. (1) Pine nuts are extensively consumed worldwide as an ingredient in different foods, in both raw and roasted form. The growing popularity and introduction of pine nuts in dishes such as tarts, pesto and gourmet salads, desserts, breads, cakes, candies, vegetarian and non-vegetarian dishes, chocolates in Europe might be a contributing element [10
]; (2) A rapid exchange of information by consumers via internet and the print media allow people to easily recognize the developing symptoms of PNS [17
]; (3) Introduction of newer (non-traditional) species of pine nuts onto the global markets [17
] as a result of competitive global trade.
The first two causes of PNS development might have given rise to the fact that many studies on pine nuts started to be done from the clinical toxicology, food and agricultural point of view. The third cause (i.e., global trade) was neglected as is evident from the dearth of studies. In our opinion, worldwide trade and the growing popularity of pine nuts in the food industry is a good opportunity for forest scientists, pathologists, and societal marketing researchers to take the initiative. The starting questions could be; which species would be good alternatives to those we already have? Which species are the most profitable? How can plantations be managed to obtain a bumper pine nuts crop? Why do a few tree species cause PNS while others do not?
Having said this, we acknowledge the fact that forest sciences research (particularly for societal marketing researchers and economists) on pine nuts might not be simple due to the lack of reliable data or a databank, which would hinder a full exploration of the trade aspects and valuation of pine nuts. However, it will be a challenge for forest pathologists and entomologists due to climate change and the increase in global trade of pine nuts, which are the main drivers of adventive insects. Table 5
summarizes the studies linked to PNS and economic valuations.
4.2.2. Pathogens and Pests of Pine Nuts
The introduction of emerging infectious diseases (EIDs) into new areas has been associated to climate change, human ecology, increased global trade and economic growth [59
]. A recent study attributed seven underlying drivers (alien pathogenic invasion, climate change, emergence of aggressive species or strains, rise in hybridization of fungi, latent and cryptic pathogens, establishment of novel links between pathogens and their vectors, adaptation of new crops and cultivation practices) of EIDs [61
]. Often more than one driver may cause a rise in the range of pathogens, insects and ultimately infectious diseases.
An increasing number of connections between adventive insects (acting as vector) and local fungi (acting as pathogen) occur in forest ecosystems [62
]. According to Ghelardini et al. [61
], establishment of novel links between pathogens and their vectors, climate change, latent and cryptic pathogens are a few of the important factors identified that cause tip-blight of pines, also called dieback, due to Diplodia sapinea
or D. pinea
and its association with an adventive insect, Leptoglossus occidentalis
Heidemann. Figure 2
shows the current presence of L. occidentalis
in the world. There are many cone and seed insects of pines mentioned in the literature. For example, Dioryctria mendacella
Staudinger, Ernobius parens
Mulsant and Rey, Ernobius impressithorax
Pic, Pissodes validirostris
Sahlberg, and L. occidentalis
]. However, L. occidentalis
is one of the most extensively studied insect vectors on pine nuts.
is a widespread pathogenic fungus also known as Sphaeropsis sapinea
or D. pinea. D. sapinea
is commonly found in Europe, South Africa and the US. It is damaging for pines both in their natural range and in plantations [69
]. D. sapinea
is badly damaging the cones of stone pine (P. pinea
) in Italy [72
]. In 2013, the first report of D. sapinea
on Scots pine (Pinus sylvestris
L.) and Austrian pine (Pinus nigra (Lodd. ex Lindl.
) came from Sweden [73
]. The conidia of D. sapinea
need L. occidentalis
for their lengthy and extensive dispersal, though primary dissemination occurs via rain splashes and wind currents [74
(Hemiptera; Heteroptera; Coreidae) is an indigenous species of the US [75
] and is commonly known as leaf-footed conifer seed bug or western conifer seed bug (WCSB). WCSB feeds on seed sap by sucking and weakens the seed or even makes it abort [76
Among numerous introduced groups of organisms in Europe, arthropods represent nearly 94% [77
]. WCSB is one of the insect species that was introduced into Europe roughly 20 years ago. It has been documented that it feeds on nearly 14 American and European conifer species: Pinus
spp., Calocedrus decurrens
(Torr.) Florin, Pseudotsuga menziesii
(Mirb.) Franco, Tsuga canadensis
(L.) Carrière, Cedrus
spp. and Picea
] are some of the important ones. WCSB was observed for the first time in western North America. After World War II, it started to spread eastwards in the US and Canada [80
]. It was recorded for the first time in Vicenza, Italy during autumn 1999 [75
Soon after its discovery in Italy, WCSB started to expand to other parts of the European continent. It can now be found in Slovenia, Croatia, Hungary, Switzerland, Austria, Germany, and Czech Republic to the north, and France to the west [88
]. In 2003, it was also independently recorded in Spain [88
]. WCSB was also found for the first time in Japan in 2009 [89
]. During 2010, it was reported in Denmark and Norway [90
]. WCSB was first recorded in Russia in 2010 (Rostov Province) and in Ukraine in 2011 (Crimea and Zaporizhia Province) as cited by Gapon [91
]. It was also first reported in Greece during 2011. The insect was collected from central Evia, Attica and the north of Peloponnese. It was mainly found on Pinus halepensis
]. Recently, some researchers confirmed the presence of WCSB in four regions of Chile i.e., Atacama, Metropolitan, Maule, and Bío Bío territories [93
In northern Italy, WCSB can complete two or three generations per year [94
]. In autumn, adults seek shelter for their overwintering activities [78
]. The adults and nymphs feed on cones and can potentially create significant economic losses in high-value seed orchards [65
]. WCSB has also been thought to deteriorate the production of pine nuts for human consumption in Italian stone pine (P. pinea
) stands. Pine nuts production is decreased by the activities of WCSB in Italy, resulting in lower income [96
] for forest owners. Furthermore, it is notorious for causing a nuisance and damage to plumbing materials when adult aggregates invade residential buildings for overwintering [84
]. This is why they are also known as urban bugs.
It is pertinent to say that beetles are usually associated as vector to plant pathogens in forests, however, this was the first time a true bug (L. occidentalis
) was observed to play a possible role as vector for D. sapinea
in a natural forest ecosystem [98
]. During 2012, Luchi et al. [98
] conducted an experiment to understand the fungus and disease outbreak mechanism. They found a correlation between the adventive L. occidentalis
and native D. sapinea
). Molecular analysis (real-time PCR) showed that D. sapinea
was present both on the bodies of L. occidentalis
and on the symptomless P. pinea
cones that were the insect’s main food source. Moreover, both organisms share similar habitat conditions. The conspicuous damage on pine trees may be explained by their co-habitation that prompts the disease spread and great invasive potential [99
The results of a research conducted by Bracalini et al. [68
] at Maremma regional park in Italy also suggested that the low cone production and high number of damaged seeds agree with an overall decline of stone pine nut production in Tuscany (Italy). The authors claim that the findings have been confirmed by the local nut producing companies [68
A fungus-insect interaction usually profits both parties [98
]. The fungus takes advantage of the insect via its dispersal to other pines or other tree species while the insect profits because the fungus may stimulate the plant to produce monoterpenes, which are responsible for entomophilic community formation. Similarly, a study on P. tabuliformis
(Chinese pine) reported that the fungus Leptographium procerum
(W.B. Kendr.) (syn. Verticicladiella procera
) raised levels of monoterpene attracting the insect Dendroctonus valens
] which acts as vector of the fungus.
Depending on climatic and environmental conditions, D. sapinea
may act as a latent pathogen enhanced by climatic stress and able to cause a speedy death of currently expanding shoots [101
]. The potential involvement of WCSB in vectoring the conidia of D. sapinea
was verified by Tamburini et al. [87
]. At present, D. sapinea
and L. occidentalis
are not listed as pests recommended for regulation of quarantine pests by the European and Mediterranean Plant Protection Organization [102