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Shrubs; Axis splits; Eccentric growth; Fragmented cambia; Growth centers

The deserts and xeric shrublands [1] are the largest terrestrial biome, covering 19% of Earth’s land surface area [2]. Among the various shrublands, precipitation is usually between 200 and 1,000 mm annually with hot, dry summers and cold, moist winters for long periods [3]. Shrublands are composed mostly of shrubs or short trees without sufficient precipitation to support tall trees [4]. Most shrubs are short, woody plants that have many stems rather than a single trunk [1]. Shrubs display abnormalities that most trees do not exhibit. The characteristics of these abnormalities need to be described.

The vascular cambium of woody plants originates between the primary xylem and primary phloem after primary growth is complete. Normally, the vascular cambium is a ring to cells that produces secondary xylem to the inside and secondary phloem to the outside. Readers are referred to Mauseth [6-8] for the process of normal vascular cambium formation and function. Many shrubs have vascular cambium abnormalities that may limit overall plant growth [9].

Two types of vascular cambium abnormalities are prevalent in shrubs. The first type is axis splitting, which occurs when an intact vascular cambium ring is fragmented by growth of surrounding tissues. A Fragmented Cambium (FC) consists of a group of intact cambium cells that are separated from other cambial cells.

The second cambium abnormality is eccentric growth. The manifestation of eccentric growth is the presence of lobes. Lobes have a convex appearance because the vascular cambium produces normal xylem cells. Each side of a lobe is concave since the vascular cambium in these two areas in non-functional.

Fragmented or groups of cambial cells from both axis splits and lobes are considered Fragmented Cambia (FC). During plant development, these fragmented groups of cells can be moved during growth of surrounding tissues. Fragmented cambial cells may be inactive from time to time. Sometime later, these fragmented cambial cells may form Growth Centers (GCs) that can produce xylem and phloem cells. Eventually, these growth centers may produce independent shoots and roots. The purpose of the current study is to document abnormal growth characteristics of shrubs.

Sample collection

All plant samples were collected in May 2021. Plants of Adenostoma fasciculatum var. fasciculatum were collected at South Fork Trail 2E17 (33.70 N, 116.76 W) along highway 74 near Mountain Center, CA, U.S.A. Plants of Artemisia california were obtained along Whitewater Canyon Road (33.95 N, 116.65 W) near Bonnie Bell, CA, U.S.A. Plants of Eriogonum fasciculatum were collected along Highway 74 near Steinoff Avenue (33 44.45 N; 117 05.94 W) in Hemet CA, U.S.A. Five plants of each species were obtained during field work. All plant names were verified using the international plant names index. Plants were air-dried, placed into shipping boxes and shipped to the laboratory for analysis.

Production of wood segments

Prior to sawing, all plants were photographed. Samples were trimmed to 5 cm above and below each crown. Plants were placed into containers and liquid paraffin wax was poured into each container. The purpose of the solidified wax is to preserve natural orientation of all plant materials throughout the process. After the wax solidified, all plant samples were sawn with a WEN saw, model 3959. Thus, the samples were sawed into wood segments embedded in solid wax. Segments were from 5 to 17 mm in thickness.

Wood segment evaluations

After sawing, segments were sanded with 600 grit sandpaper. Prior to photography, segments were brushed with water to improve xylem ring visibility.

Photographic evaluations

Each surface was photographed with a Canon Power Shot ELPH100HS camera with a ruler in the frame to ensure accurate measurements. For each plant, the photograph of the segment at the transition zone was evaluated first. Thereafter, segments above and below the transition zone were evaluated. As described above, there are two types of Growth Centers (GCs). One type is the peripheral area of each convex lobe while the second is the peripheral area of a ring of concentric xylem cells. Areas of dead cells were also identified. In many cases, independent structures could not be identified as either roots or shoots.

Samples of the three species of this study have been published elsewhere. The samples described herein are excellent examples of the growth abnormalities described above.

Adenostoma fasciculatum

The sample of Adenostoma fasciculatum exhibited an axis split, many eccentricities, a large area of dead tissues and the generation of more than 23 GCs. Many individual stems were produced over a distance of 52.8 mm from the transition zone (Figure 1 and Table 1). The segment 15 mm below the transition zone had one large root and many smaller roots with 21 GCs. The large root had many lobes with dead tissues in the central area (Figure 1A). The segment 9.0 mm above the transition zone had many separated sections with many lobes and dead tissues in the central area, with at least 20 GCs present (Figure 1B). In the segment 17.0 mm above the transition zone, the sections showed in the previous segment were spread more laterally, with two shoots and a large area of dead tissues present (Figure 1C). The segment at 27.0 mm had more dead tissues than previous segments (Figure 1D). The segment at 43.0 mm had 23 GCs with many stems radiating laterally, with many dead tissues present (Figure 1). The top of all segments had a large number of individual stems and possibly some roots (Figure 1F).

 

Figure 1: Segments of Adenostoma fasciculatum. A) Segment 15 mm below the transition zone had one large root and many smaller roots. The large root had many lobes with dead tissues in the central area. B) Segment 9.0 mm above the transition zone had many separated sections with many lobes and dead tissues in the central area. C) Segment 17.0 mm above the transition zone with shoots spread more laterally and a large area of dead tissues present. D) Segment at 27.0 mm had more dead tissues than previous segments. E) Segment at 43.0 mm had 23 GCs with many stems radiating laterally, with many dead tissues present. F) Top view of all segments had a large number of individual stems and possibly some roots.

Table 1: Characteristics of samples of Arctostaphylos glauca.

Artemisia californica

The first of three samples of Artemisia californica exhibited eccentricities, an axis split, dead tissues, lobes and the production of at least 17 GCs between the transition zone and 34 mm above the transition zone (Figure 2 and Table 2). The segment at the transition zone had only one GC with limited secondary growth (Figure 2A). The segment at 11.9 mm above the transition zone had seven GCs with small stems emerging from the main stem (Figure 2B). At 25.9 mm, evidence of a previous axis split is present since the GCs are spread from the central portion that has a large area of dead tissues. Fourteen GCs were present (Figure 2C). The segment at 33.9 mm above the transition zone had at least 17 GCs in independent stems with a large area of dead tissues (Figure 2). The top view had at least 15 independent stems (segment not showed).

 

Figure 2: Segments of Artemisia californica. A) Segment at the transition zone had only one GC with limited secondary growth. B) Segment at 11.9 mm above the transition zone had seven small stems emerging from the main stem. C) Segment at 25.9 mm had evidence of a previous axis split since the GCs are spread from the central portion that has a large area of dead tissues. D) Segment at 33.9 mm above the transition zone had at least 17 GCs in independent stems with a large area of dead tissues.

Table 2: Characteristics of samples of Artemisia californica.

The second sample of Artemisia californica exhibited an axis split, several eccentricities, dead tissues and the production of at least nine GCs between the transition zone and 25 mm above the transition zone (Figure 3 and Table 2). An axis split with several lobes indicating eccentric growth capable of generating many GCs occurred at the transition zone (Figure 3A). The segment 13 mm above the transition zone showed nine GCs with a large central area of dead tissues. The axis split in the segment at the transition zone generated GCs in this segment (Figure 3B). Nine independent stems with some smaller stems and dead tissues in the central area were present at 25.0 mm above the transition zone (Figure 3C). The top of these segments, at 37.0 mm above the transition zone, had several large and many small stems (Figure 3).

 

Figure 3: Segments of Artemisia californica. A) Segment at the transition zone with an axis split with several lobes indicating eccentric growth. B) Segment 13 mm above the transition zone had nine GCs with a large central area of dead tissues. C) Segment at 25.0 mm above the transition zone had nine independent stems with some smaller stems and dead tissues in the central area. D) Segment at 37.0 mm above the transition zone, had several large and many small stems.

The third sample of Artemisia californica exhibited an axis split, many eccentricities, dead tissues and the production of at least 18 GCs between the transition zone and 30 mm above the transition zone (Figure 4 and Table 2). An axis split with at least six growth centers represented by six lobes occurred at the transition zone. Dead tissues were present in the central area where an axil split occurred (Figure 4A). The segment at 7.0 mm above the transition zone had at least nine GCs and at least one independent shoot. Dead tissues were present in the central area (Figure 4B). Many GCs and a large area of dead tissues were present at 17 mm (Figure 4C). At 30 mm above the transition zone, 18 independent shoots were present (Figure 4).

 

Figure 4: Segments of Artemisia californica. A) Segment at the transition zone had an axis split with at least six growth centers represented by six lobes. Dead tissues were present in the central area where an axil split occurred. B) Segment at 7.0 mm above the transition zone had at least nine GCs and at least one independent shoot. Dead tissues were present in the central area. C) Segment at 17 mm had many GCs and a large area of dead tissues. D) Segment at 30 mm above the transition zone had 18 independent shoots.

Eriogonum fasciculatum

The sample of Eriogonum fasciculatum had evidence of an axis split, eccentricities and dead tissues prior to production of stems over the distance of 43.7 mm above the transition zone (Figure 5 and Table 3). The sample at the transition zone (not shown) had an axis split. Evidence of the axis split is seen in the segment 6.8 mm above the transition zone, since many roots and shoots are dispersed with dead tissues in the center (Figure 5A). This segment had at least 25 growth centers with eccentric growth. The segment at 20.8 mm had large roots and shoots with many lobes and dead tissues (Figure 5B). Widespread shoots with a large area of dead tissues occurred at 38.9 mm above the transition zone (Figure 5C). Stems of various sizes were present in the top segments, 43.7 mm above the transition zone (Figure 5D).

 

Figure 5: Segments of Eriogonum fasciculatum. A) Segment at 6.8 mm above the transition zone with evidence of a previous axis split in which many roots and shoots are dispersed with dead tissues in the center with at least 25 growth centers with eccentric growth. B) Segment at 20.8 mm had large roots and shoots with many lobes and dead tissues. C) Segment at 38.9 mm above the transition zone had many shoots with a large area of dead tissues. D) View of top segment 43.7 mm above the transition zone had stems of various sizes.

Table 3: Characteristics of samples of Eriogonum fasciculatum.

Axis splits are a common, almost defining characteristics of growth form in desert shrubs. Schenk reviewed mechanisms and patterns of axis splits and described the many ecological functions of axis splits in desert shrubs. Axis splits are important with regard to xylem redundancies. More on this aspect later.

As stated previously, axis splits only occur during the initial stage of secondary growth in roots and shoots. If the cambium remains relatively intact and does not split during the initial stage, it will produce secondary xylem and secondary phloem. The presence of these tissues may assist in the long-term maintenance of an intact vascular cambium.

Eccentric growth is common in many shrub species of the western United States. Many Artemisia species species of Purshia, Coleogyne ramosissima, Encelia californica, Sarcobatus vermiulatus Adenostoma fasciculatum, Arctostaphylos glauca, Artemisia californica, Eriogonum fasciculatum, Heteromeles arbutifolia, Frangula californica and Eucalyptus nicholii show extensive eccentricities along all stems. As mentioned previously, eccentric growth occurs when vascular cambium functions normally in some portions of a stem and not in neighboring portions. This situation produces lobes in which the cambium on the convex portions of the lobes are certainly growth centers. If external forces eventually impact these lobes, the vascular cambium may become fragmented and move to other locations to act as growth centers there. Eccentric growth seems to be independent of axis splitting, although both can occur in the same tissues.

Besides axis splitting and xylem eccentricities, many other abnormalities occur with the vascular cambium in woody plants. Growth anomalies caused by an abnormal vascular cambium include regenerating cambia, supernumerary cambia, unequal cambial activity, successive cambia and fasciations.

Wood eccentricities have been most studied in Artemisia tridentata and Coleogyne ramosissima. These eccentricities may adversely affect their ability to resist bending stresses and in turn, lead to stem failure. A study of stems of Artemisia tridentata revealed an apparent enigma. On one hand, data from older plant stems showed an increase in annual xylem rings for every 2 mm of stem growth. This result suggests that growth of main stems was only 2 mm per year. On the other hand, stem terminals may grow up to 18 cm during each growing season (Figure 6A). This extraordinary terminal growth provides for the formation of many seeds on branches of terminals by the end of each growing season. Branches may produce up to 1,000 seeds per terminal (Figure 6). Other research demonstrated that wood eccentricities on main stems were very prevalent at many nodes of these branches. The entire weight of these large seed masses on branches of main stems with the presence of wood eccentricities on main stems at branches may contribute to a lower resist to stem bending so many main stems may fail. Failing at terminals may account for the low overall growth rate of stems.

 

Figure 6: Two view of plants of Artemisia tridentata. A) View of an entire plant with many inflorescences. Note the many long terminals. Taken from www.pinterest.com. B) View of a single inflorescence with many seeds. Taken from ar.inspiredpensil.com.

For many plant groups, the path of woodiness was quite long and not always direct. For some woody plant groups, woodiness may not be completely adaptive and being no longer necessary, there is a tendency for woodiness to become lost and herbaceous again. Once lost the first time, regaining woodiness may take a long time. Species of Artemisia and other species in the Asteraceae probably came from ancestors that were shrubby, much of the family is herbaceous and Artemisia may have descended from ancestors that were not woody. These factors may contribute to eccentric xylem in Artemisia. Possibly, similar characteristics may contribute to eccentric and axis splitting in other shrub species.

Many areas of the earth are experiencing extreme and long-term droughts. Southern Africa has experienced the worst drought on record. China has experienced the worst drought in 60 years. The western United States has recently experienced the worst drought in 1200 years.

Shrubs are particularly well adapted to survive droughts. Embolisms may develop in some stems during droughts so these stems will die. However, embolisms that develop in one stem do not affect other stems. The production of multiple shoots and roots via GCs in crowns of shrubs may provide hydraulic redundancy. If embolisms develop in some shoots and roots and they die during long-term droughts, GCs may generate future shoots and roots to replace these dead tissues.

In a likewise manner, shrubs may be well adapted to survive wildfires. During 2023, wildfires in Canada covered 18 million ha. Wildfires are widespread throughout China. In 2020, California had the largest fire season on record with over 1,770,000 ha burned. In the United States, more financial damage to structures occurs from wildfires of shrubs and grasslands than from wildfires of forests.

The many GCs that are deeply embedded in the crowns of shrubs may contribute to the revival of plants after wildfires in Australia and the United States. There is no direct data to support the idea that GCs in shrubs are responsible for revival of shrubs after wildfires. There is ample evidence to show that shrubs revive after wildfires. The embedded GCs in crowns of shrubs may contribute to revival of plants after wildfires.

Shrubs live in hot dry summers and cold winters with low moisture conditions. Shrubs exhibit a high level of xylem abnormalities. Axis splitting and eccentricity growth are common. Axis splits provide an effective method to produce many stems. Axis splits produce fragmented cambia that lead to growth centers. Growth centers can provide recovery from long term droughts and wildfires. Eccentric growth of xylem cells may lead to weakened stems. Limited heights of shrubs may be caused by weakened stems. Although abnormalities occur in xylem cells of roots and stems of shrubs, shrub species have high reproductive rates and survival rates.

1. Newman IV (1956) . Phytol 1-19.

   []

2. Dobbins DR (1971) Am J Bot 58: 697-705.

   [] []

3. Fahn A (1964) Some anatomical adaptations of desert plants. Phytol 4: 93-101.
4. Evans LS (2022) . Rhizosphere 24: 100584.

   [] []

5. Evans LS (2022) . J Torrey Bot Soc 150: 331-344.

   []

6. Evans LS (2023) . Rhizosphere 25: 100663.

   [] []

7. Evans LS (2024) . J Torrey Bot Soc 151: 51-64.

   []

8. Kingsley MA (1911) Bull Torrey Bot Club 38: 307-317.

   [] []

9. Ginzburg C (1963) Some anatomic features of splitting of desert shrubs. Phytol 13: 92-97.