Amphioxus Feeding & Respiration

Cross references:    Amphioxus   Amphioxus Behavior     Endostyle = Thyroid  
Amphioxus Gut Hormones   Amphioxus Smell   Amphioxus Taste     Amphioxus Gut Nerves   
Lamprey Rhombencephalon   

I had hypothesized that, for filter feeders such as the amphioxus, feeding and respiration take place simultaneously.    It turns out that this is true for the lamprey but not for the amphioxus. 

    relevant references fromLamprey Rhombencephalon   

55<144    1999  
An anatomical study of brainstem projections to the trigeminal motor nucleus of lampreys   
This study concentrates on the labeled neurons in the rhombencephalon, since the essential circuits for mastication and swallowing are confined to this region in higher vertebrates."  
    My comment
Perhaps the anatomy for feeding is even more ancient than the anatomy for locomotion.  

40<144    2004       
Free PMC Article   
Organization of higher-order brain areas that initiate locomotor activity in larval lamprey.   
These new results suggest that neurons in the RLR project rostrally to locomotor areas in the DLM and VMD."  
    My comment
This postulates communication from lower to higher levels, which is opposite of my basic assumption. 
    See:  Initiation of Locomotion in Lampreys  for full Abstract, Related citations and Cited by's. 

23<144    2007 
Respiratory rhythms generated in the lamprey rhombencephalon.  
Our results support the hypothesis that normal breathing depends on the activity of neurons located in the rostral rhombencephalon in lampreys, whereas the caudal rhombencephalon generates the slow pattern."  
    See also:  3<144, below.  2013  Neuronal mechanisms of respiratory pattern generation are evolutionary conserved.

3<144    2013 
Neuronal mechanisms of respiratory pattern generation are evolutionary conserved.  
A brainstem region, the paratrigeminal respiratory group (pTRG), has been suggested to play a crucial role in the respiratory rhythm generation in lampreys. ... pTRG neurons projecting to the vagal motoneuronal pool were identified in a restricted area of the rostral rhombencephalon at the level of the isthmic Müller cell I1 close to sulcus limitans of His."  
    My comments
1.  What is the "vagal motoneuronal pool" and where is it located?  This may be more fundamental to behavior than the previously identified reticular neurons.  
2.  See: 23<144, above.  2007  Respiratory rhythms generated in the lamprey rhombencephalon, above.   

    new links

Lancelet - Wikipedia   
Lancelets have no respiratory system, breathing solely through their skin, which consists of a simple epithelium. Despite the name, little if any respiration occurs in the gill slits, which are solely devoted to feeding. The circulatory system does resemble that of primitive fish in its general layout, but is much simpler, and does not include a heart. There are no blood cells, and no haemoglobin.[8] "    

Searching Google for "amphioxus respiration feeding" found 31,300 references  

Cilliary Mechanisms on the Gill and Mode of Feeding of Amphioxus       
31-page PDF which I was unable to copy and paste but which is available online for free. 
It expresses the opinion that the gills are used almost exclusively for feeding, not respiration. 

Filter Feeding in Lancelets (Amphioxus), Branchiostoma lanceolatum   
Full length, highly detailed discussion of feeding, with figures, available online for free.  No mention of respiration. 

Morphometric partitioning of respiratory surfaces in amphioxus - 3381.full.pdf   
    My comments
As is so common for PDFs, it was necessary to download the entire document in order to copy-and-paste from it.  
    "The anatomical diffusing factors (ADFs), defined as the ratio of surface area to the thickness of the diffusion barrier, of possible respiratory surfaces of adult amphioxus (Branchiostoma lanceolatum) were evaluated using stereological methods.  
    The ADF is greatest for the lining of the atrium and for the skin covering the segmental muscles. Calculation of the diffusing capacities for O2 revealed that the lining of the atrium makes up nearly 83 % of the entire diffusing capacity (8.86´10-3 mlmin-1mg-1 kPa-1) while the skin over the segmental muscles (9 %), the skin over the metapleural fold (4 %) and the gill bars (4 %) are of minor importance.  
    The diffusing capacity of surfaces lying over coelomic cavities makes up 76 % of the whole diffusing capacity, which is consistent with the hypothesis that the coelom may function as a circulatory system for respiratory gases. Muscles have approximately 23 % of the entire diffusing capacity, indicating that they may be selfsufficient for O2 uptake. The diffusing capacity of the blood vessels in the gill bars is only 1% of the total.  
    Thus, the ‘gills’ lack significant function as respiratory organs in amphioxus (lancelets).  Our results refute the hypothesis that the gill bars are of major importance for respiration in amphioxus.
Key words:
    amphioxus, Branchiostoma lanceolatum, anatomical, diffusing factor, diffusing capacity, oxygen uptake, respiratory
organ, lancelet 
    "In craniates, including the filter-feeding ammocetes larvae of lampreys, the gills are the main respiratory organ. The craniate gill structure is radically different from the ciliated gill bars of amphioxus, and the question arises as to whether such a major structural conversion could have occurred in an organ that is necessary for such a vital function as respiration." 
    Phylogenic significance
    "The implications of the present study for a filter feeder as the common ancestor of amphioxus and vertebrates are intriguing. While not able to provide anatomical details of the transition to gill breathing, functional anatomical analyses such as this can point out functional constraints that could make one pathway of evolution more probable than another. If, as in amphioxus, the atrial surface of the vertebrate ancestor rather than the gill bars themselves were the respiratory exchanger, then a stepwise modification of the gill structures can be envisioned. The ventilatory motor could be changed from cilia to a velum, and expanded surfaces could develop in the gills while leaving the filter-feeding mechanism intact, as in the ammocetes larva (Mallat, 1984). Such a major modification would be difficult to envision if the gills were the major respiratory organ. However, the rudiments of a vertebrate circulatory system are present, which, given an increased respiratory gill function, could supply the body tissues with O2" 

    Brief but informative full length course summary available online for free.    
The interior of the ventral half of the section is occupied by the pharynx.  

Figure 1. Juvenile Branchiostoma, cleared specimen. Cephchord16L.gif

  Figure 1

Its lumen is surrounded by the gill bars, appearing here in oblique section.   In living material the gill bars are nearly vertical but in most fixed specimens the pharynx is distorted so that the bars are aligned obliquely or nearly horizontally.   As a consequence you see them in oblique or cross section rather than sliced along their long axis as you might have expected.   Look closely at the circle of gill bars noting first the gill slits that separate them.   It is through these slits that water passes during feeding.   Examine some of the gill bars with 400X (careful!) and note the abundance of cilia on their inner margins.   Lateral cilia (Fig 3, 29-3C) are located on the surfaces between the gill bars and generate the feeding current which passes from the pharynx lumen through the gill slits to the atrium.   In contrast frontal cilia are on the inner surface of the gill bars face the lumen and are responsible for transporting food and mucus dorsally to the esophagus. Each gill bar is associated with a small coelomic space and an aortic arch but these are difficult to see.   

Figure 2. Anterior end of a cleared juvenile Branchiostoma. Cephchord17L.gif

Figure 2

            Ventrally along the pharynx there is a longitudinal, median, ciliated groove, the endostyle, which secretes a copious mucus.   The mucus contains iodine and the endostyle is homologous to the vertebrate thyroid gland (positional and intermediates criteria).   Look at the endostyle with high power to find its cilia.   Ventral to the endostyle there is a small endostylar coelom surrounding an even smaller ventral aorta.   The endostylar coelom is homologous to the pericardial coelom of vertebrates.

            Dorsally in the pharynx there is another median furrow, the epibranchial groove.   The paired dorsal aortae are located dorsolateral to it.   Most of the space surrounding the pharynx is the atrium, which is enclosed by an ectodermal epithelial lining.  

            During feeding the lateral cilia of the gill bars generate a water current that enters the pharynx through the mouth.   The water passes laterally through the gill slits, out of the pharynx, and into the surrounding atrium.   Mucus secreted by the endostyle is carried upward over the inner surface of the gill bars by ciliary currents generated by frontal cilia.   The mucus entangles food particles attempting to pass between the gill bars and transports them to the epibranchial groove.   The cilia of the groove then move the mucus and trapped food posteriorly into the esophagus.  Food is moved through the gut by its ciliated walls. The epithelium of the hepatic cecum secretes digestive enzymes into the gut lumen.   Digestion occurs extracellularly in the stomach and iliocolon and its products are absorbed by the epithelium of the cecum.

            Although inconspicuous, the cephalochordate coelom occupies its expected position surrounding the gut (Fig 29-3C, 29-9).   Fairly large perivisceral coelomic spaces may be seen lying dorsolateral to the pharynx.   Extensions of this part of the coelom extend to the gill bars and are continuous with the coelom in those structures."